Rescue of the cardiac defect in erbB2 mutant mice reveals essential roles of erbB2 in peripheral nervous system development

Neuron

Volumn 23, Issue 2, 1999, Pages 273-283

  Morris, Jacqueline K ^a   Weichun, Lin ^a   Hauser, Chris ^a   Marchuk, Yelena ^a   Getman, Damon ^a   Kuo Fen, Lee ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; CHOLINERGIC RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; NEU DIFFERENTIATION FACTOR; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; DIAPHRAGM MUSCLE; EMBRYO; FASCICULATION; MOTONEURON; MOUSE; NERVE FIBER DEGENERATION; NERVE FIBER GROWTH; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL; SENSORY NERVE CELL; SIGNAL TRANSDUCTION;

EID: 0033152451     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80779-5     Document Type: Article

References (66)

1. Altiok, N., Bessereau, J.-L., and Changeux, J.-P. (1995). ErbB3 and ErbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: Differential expression at the endplate. EMBO J. 14, 4258-4266.
2. Apel, E.D., Glass, D.J., Moscoso, L.M., Yancopoulos, G.D., and Sanes, J.R. (1997). Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18, 623-635.
3. Bhattacharyya, A., Brackenbury, R., and Ratner, N. (1994). Axons arrest the migration of Schwann cell precursors. Development 120, 1411-1420.
4. Britsch, S., Li, L., Kirchhoff, S., Theuring, F., Brinkman, V., Birchmeier, C., and Riethmacher, D. (1998). The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev. 12, 1825-1836.
5. Bunge, R.P. (1993). Expanding roles for the Schwann cell: Ensheathment, myelination, trophism and regeneration. Curr. Opin. Neurobiol. 3, 805-809.
6. Burden, S.J. (1998). The formation of neuromuscular synapses. Genes Dev. 12, 133-148.
7. Burden, S., and Yarden, Y. (1997). Neuregulins and their receptors: A versatile signaling module in organogenesis and oncogenesis. Neuron 18, 847-855.
8. 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.J., and Gearing, D. (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.
9. Carpenter, E.M., and Hollyday, M. (1992). The location and distribution of neural crest-derived schwann cells in developing peripheral nerves in the chick forelimb. Dev. Biol. 150, 144-159.
10. Carraway, K.L., III, and Cantley, L.C. (1994). A neu acquaintance for erbB3 and erbB4: A role for receptor heterodimerization in growth signaling. Cell 78, 5-8.
11. Carraway, K.L., III, Weber, J.L., Unger, M.J., Ledesma, J., Yu, N., Gassmann, M., and Lai, C. (1997). Neuregulin-2, a new ligand of Erb3/Erb4-receptor tyrosine kinases. Nature 387, 512-516.
12. Chang, H., Riese, D.J., II, Gilbert, W., Stern, D.F., and McMahan, U.J. (1997). Ligands for ErbB-family receptors encoded by a neuregulin-like gene. Nature 387, 509-512.
13. Colman, D.R. (1997). Neurites, synapses, and cadherins reconciled. Mol. Cell. Neurosci. 10, 1-6.
14. 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., et al. (1996). The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 510-512.
15. Dong, Z., Brennan, A., Liu, N., Yarden, Y., Lefkowitz, G., Mirsky, R., and Jessen, K. (1995). Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation and maturation of rat Schwann precursors. Neuron 15, 589-596.
16. Erickson, S.L., O'Shea, K.S., Ghaboosi, N., Loverro, L., Frantz, G., Bauer, M., Lu, L.H., and Moore, M.W. (1997). ErbB3 is required for normal cerebellar and cardiac development: A comparison with ErbB2 and heregulin-deficient mice. Development 124, 4999-5011.
17. Falls, D.L., Rosen, K.M., Corfas, G., Lane, W.S., and Fischbach, G.D. (1993). ARIA, a protein that stimulates actylcholine receptor synthesis, is a member of the neu ligand family. Cell 72, 801-815.
18. Fischbach, G.D., and Rosen, K.M. (1997). ARIA: A neuromuscular junction neuregulin. Annu. Rev. Neurosci. 20, 429-458.
19. Frank, E., and Sanes, J.R. (1991). Lineage of neurons and glia in chick dorsal root ganglia: Analysis in vivo with a recombinant retrovirus. Development 111, 895-908.
20. Gassmann, M., Casagranda, F., Orioli, D., Simon, H., Lai, C., Klein, R., and Lemke, G. (1995). Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378, 390-394.
21. Gautam, M., Noakes, P.G., Moscoso, L., Rupp, F., Scheller, R.H., Merlie, J.P., and Sanes, J.R. (1996). Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
22. Gautam, M., Noakes, P.G., Mudd, J., Nichol, M., Chu, G.C., Sanes, J.R., and Merlie, J.P. (1995). Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377, 232-236.
23. Harrison, R.G. (1924). Neuroblast versus sheath cell in the development of peripheral nerves. J. Comp. Neurol. 37, 123-205.
24. Hayes, C., Kelly, D., Murayama, S., Komiyama, A., Suzuki, K., and Popko, B. (1992). Expression of the neu oncogene under the transcriptional control of the myelin basic protein gene in transgenic mice: Generation of transformed glial cells. J. Neurosci. Res. 31, 175-187.
25. Ho, W.-H., Armanini, M.P., Nuijens, A., Phillips, H.S., and Osheroff, P.L. (1995). Sensory and motor neuron-derived factor. J. Biol. Chem. 270, 14523-14532.
26. erbB2. Science 256, 1205-1210.
27. Jessen, K.R., and Mirsky, R. (1991). Schwann cell precursors and their development. Glia 4, 185-194.
28. Jin, J.-J., Nikitin, A.Y., and Rajewsky, M.F. (1993). Schwann cell lineage-specific neu (erbB-2) gene expression in the developing rat nervous system. Cell Growth Diff. 4, 227-237.
29. Jo, S.A., Zhu, X., Marchionni, M.A., and Burden, S.J. (1995). Neuregulins are concentrated at nerve-muscle synapses and activate ACh- receptor gene expression. Nature 373, 158-161.
30. Kaplan, M.R., Meyer-Franke, A., Lambert, S., Bennett, V., Duncan, I.D., Levinson, S.R., and Barres, B.A. (1997). Induction of sodium channel clustering by oligodendrocytes. Nature 386, 724-728.
31. Karnovsky, M.J. (1964). The localization of cholinesterase activity in rat cardiac muscle by electron microscopy. J. Cell Biol. 23, 217-232.
32. Keynes, R.J. (1987). Schwann cells during neural development and regeneration: Leaders or followers? TINS 10, 137-139.
33. Kramer, R., Bucay, N., Kane, D.J., Martin, L.E., Tarpley, J.E., and Theill, L.E. (1996). Neuregulins with an Ig-like domain are essential for mouse myocardial and neuronal development. Proc. Natl. Acad. Sci. USA 93, 4833-4838.
34. Kuhlbrodt, K., Herbarth, B., Sock, E., Hermans-Borgmeyer, I., and Wegner, M. (1998). Sox10, a novel transcriptional modulator in glial cells. J. Neurosci. 18, 237-250.
35. Lawson, S.N., and Biscoe, T.J. (1979). Development of mouse dorsal root ganglia: An autoradiographic and quantitative study. J. Neurocytol. 8, 265-274.
36. Lee, K.-F., Simon, H., Chen, H., Bates, B., Hung, M.-C., and Hauser, C. (1995). A requirement of the neuregulin receptor erbB2 in neural and cardiac development. Nature 378, 394-398.
37. Lewin, G.R., and Barde, Y.-A. (1996). Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
38. Liu, X., Hwang, H., Cao, L., Buckland, M., Cunningham, A., Chen, J., Chien, K.R., Graham, R.M., and Zhou, M. (1998). Domain-specific gene disruption reveals critical regulation of neuregulin signaling by its cytoplasmic tail. Proc. Natl. Acad. Sci. USA 95, 13024-13029.
39. Mahanthappa, N.K., Anton, E.S., and Matthew, W.D. (1996). Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth. J. Neurosci. 16, 4673-4683.
40. Marchionni, M.A., Marchionni, M.A., Goodearl, A.D., Chen, M.S., Bermingham-McDonogh, O., Kirk, C., Hendricks, M., Danehy, F., Misumi, D., Sudhalter, J., et al. (1993). Glia growth factors are alternatively spliced erB2 ligands expressed in the nervous system. Nature 362, 312-318.
41. Meier, T., Masciulli, F., Moore, C., Schoumacher, F., Eppenberger, U., Denzer, A.J., Jones, G., and Brenner, H.R. (1998). Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins. J. Cell Biol. 141, 715-726.
42. Meyer, D., and Birchmeier, C. (1995). Multiple essential functions of neuregulin in development. Nature 378, 386-390.
43. Moscoso, L.M., Chu, G.C., Gautam, M., Noakes, P.G., Merlie, J.P., and Sanes, J.R. (1995). Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/heregulin, and its putative receptors, ErbB2 and ErbB3, in developing mammalian muscle. Dev. Biol. 772, 158-169.
44. Noakes, P.G., and Bennet, M. (1987). Growth of axons into developing muscles of the chick forelimb is proceded by cells that stain with Schwann cell antibodies. J. Comp. Neurol. 259, 330-347.
45. Noakes, P.G., Bennett, M.R., and Davey, D.F. (1983). Growth of segmental nerves to the developing rat diaphragm: Absence of pioneer axons. J. Comp. Neurol. 218, 365-377.
46. Noakes, P.G., Bennett, M.R., and Stratford, J. (1988). Migration of Schwann cells and axons into developing chick forelimb muscles following removal of either the neural tube or the neural crest. J. Comp. Neurol. 277, 214-233.
47. Noakes, P.G., Phillips, W.D., Hanley, T.A., Sanes, J.R., and Merlie, J.P. (1993). 43k protein and acetylcholine receptors colocalize during the initial stages of neuromuscular synapse formation in vivo. Dev. Biol. 155, 275-280.
48. Peles, E., Bacus, S.S., Koski, R.A., Lu, H.S., Wen, D., Ogden, S.G., Levy, R.B., and 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.
49. Pfrieger, F.W., and Barres, B.A. (1996). New views on synapse-glia interactions. Curr. Opin. Neurobiol. 6, 615-621.
50. Pfrieger, F.W., and Barres, B.A. (1997). Synaptic efficacy enhanced by glial cells in vitro. Science 277, 1684-1686.
51. Piette, J., Huchet, M., Houzelstein, D., and Changeux, J.-P. (1993). Compartmentalized expression of the α- and γ- subunits of the acetylcholine receptor in recently fused myofibers. Dev. Biol. 157, 205-213.
52. Qiu, Y., Ravi, L., and Kung, H.-J. (1998). Requirement of ErbB2 for signaling by interleukin-6 in prostate carcinoma cells. Nature 393, 83-85.
53. Riethmacher, D., Sonnenberg-Riethmacher, E., Brinkmann, V., Yamaai, T., Lewin, G.R., and Birchmeier, C. (1997). Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 389, 725-730.
54. Sandrock, A.W., Dryer, S.E., Rosen, K.M., Gozani, S.N., Kramer, R., Theill, L.E., and Fischbach, G.D. (1997). Maintenance of acetylcho- line receptor number by neuregulins at the neuromuscular junction in vivo. Science 276, 599-603.
55. Schaeren-Wiemers, N., and Gerfin-Moser, A. (1993). 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, 431-440.
56. Schneider-Maunoury, S., Seitanidou, T., Charnay, P., and Lumsden, A. (1997). Segmental and neuronal architecture of the hindbrain of Krox-20 mouse mutants. Development 124, 1215-1226.
57. Shah, N.M., Marchionni, M.A., Isaacs, I., Stroobant, P., and Anderson, D.J. (1994). Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77, 349-360.
58. Sliwkowski, M.X., Schaefer, G., Akita, R.W., Lofgren, J.A., Fitzpatrick, V.D., Nuijens, A., Fendly, B.M., Cerione, R.A., Vandlen, R.L., and Carraway, K.L., III (1994). Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin. J. Biol. Chem. 269, 14661-14665.
59. Son, Y.-J., Trachtenberg, J.T., and Thompson, W.J. (1996). Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. TINS 19, 280-284.
60. Subramaniam, A., Jones, W.K., Gulick, J., Wert, S., Neumann, J., and Robbins, J. (1991). Tissue-specific regulation of the α-myosin heavy chain gene promoter in transgenic mice. J. Biol. Chem. 266, 24613-24620.
61. Trachtenberg, J.T., and Thompson, W.J. (1997). Nerve terminal withdrawal form rat neuromuscular junctions induced by neuregulin and Schwann cells. J. Neurosci. 17, 6243-6255.
62. Weinmaster, G., Roberts, V.J., and Lemke, G. (1991). A homolog of Drosophila Notch expressed during mammalian development. Development 773, 199-205.
63. Wen, D., Peles, E., Cupples, R., Suggs, S.V., Bacus, S.S., Luo, Y., Trail, G., Hu, S., Silbiger, S.M., Levy, R.B., et al. (1992). Neu differentiation factor: A transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell 69, 559-572.
64. Yang, X., Kuo, Y., Devay, P., Yu, C., and Role, L. (1998). A cysteinerich isoform of neuregulin controls the level of expression of neuronal nicotinic receptor channels during synaptogenesis. Neuron 20, 255-270.
65. Zhang, D., Sliwkowski, M.X., Mark, M., Frantz, G., Akita, R., Sun, Y., Hillan, K., Crowley, C., Brush, J., and Godowski, P.J. (1997). Neuregulin-3 (NRG3): A novel neural tissue-enriched protein that binds and activates ErbB4. Proc. Natl. Acad. Sci. USA 94, 9562- 9567.
66. Zhu, X., Lai, C., Thomas, S., and Burden, S. (1995). Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses. EMBO J. 14, 5842-5848.