Axonal neuregulin signals cells of the oligodendrocyte lineage through activation of HER4 and Schwann cells through HER2 and HER3

Journal of Cell Biology

Volumn 137, Issue 1, 1997, Pages 211-220

  Vartanian, Timothy ^a   Goodearl, Andrew ^a   Viehöver, Andrea ^a   Fischbach, Gerald ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEU DIFFERENTIATION FACTOR;

ARTICLE; CELL ISOLATION; CELL PROLIFERATION; CELL SURVIVAL; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MEMBRANE POTENTIAL; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SCHWANN CELL; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; ASTROCYTES; AXONS; CELL LINEAGE; GANGLIA, SPINAL; GLYCOPROTEINS; NERVE FIBERS, MYELINATED; NEUREGULINS; NEURONS, AFFERENT; OLIGODENDROGLIA; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; SCHWANN CELLS; SCIATIC NERVE; SIGNAL TRANSDUCTION; STEM CELLS; TYROSINE;

EID: 0030985765     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.1.211     Document Type: Article

References (74)

1. Barres, B.A., I.K. Hart, H.S. Coles, J.F. Burne, J.T. Voyvodic, W.D. Richardson, and M.C. Raff. 1992. Cell death and control of cell survival in the oligodendrocyte lineage. Cell. 70:31-46.
2. Barres, B.A., R. Schmid, M. Sendnter, and M.C. Raff. 1993. Multiple extra-cellular signals are required for long-term oligodendrocyte survival. Development (Camb.). 118:283-295.
3. Barres, B.A., M.C. Raff, F. Gaese, I. Bartke, G. Dechant, and Y.A. Barde. 1994. A crucial role for neurotrophin-3 in oligodendrocyte development. Nature (Lond.). 367:371-375.
4. Ben, B.N., and Y. Yarden. 1994. Neu differentiation factors: a family of alternatively spliced neuronal and mesenchymal factors. Proc. Soc. Exp. Biol. Med. 206:221-227.
5. Bunge, M.B., R.P. Bunge, D.J. Carey, C.J. Cornbrooks, C.F. Eldridge, A.K. Williams, and P.M. Wood. 1983. Axonal and nonaxonal influences in Schwann cell development. In Developing and Regenerating Vertebrate Nervous Systems. P. Coates, R. Markwald, and A. Kenny, editors. Alan R. Liss, New York. 71-105.
6. Canoll, P.D., J.M. Musacchia, R. Hardy, R. Reynolds, M. Marchionni, and J.L. Salzer. 1996. GGF/Neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron. 17:229-243.
7. Carraway, K., and S.J. Burden. 1995. Neuregulins and their receptors. Curr. Opin. Neurobiol. 5:606-612.
8. Carraway, K., M.X. Sliwkowski, R. Akita, J.V. Platko, P.M. Guy, A. Nuijens, A.J. Diamonti, R.L. Vandlen, L.C. Cantley, and R.A. Cerione. 1994. The erbB3 gene product is a receptor for heregulin. J. Biol. Chem. 269:14303-14306.
9. Coussens, L., F.T. Yang, Y.C. Liao, E. Chen, A. Gray, J. McGrath, P.H. Seeburg, T.A. Libermann, J. Schlessinger, U. Francke, et al. 1985. Tyrosine kinase receptor with extensive homology to EGF receptor shares chromosomal location with neu oncogene. Science (Wash. DC). 230: 1132-1139.
10. DiStefano, P.S., B. Friedman, C. Radziejewski, C. Alexander, P. Boland, C.M. Schick, R.M. Lindsay, and S.J. Wiegand. 1992. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron. 8:983-993.
11. Dong, Z., A. Brennan, N. Liu, Y. Yarden, G. Lefkowitz, R. Mirsky, and K.R. Jessen. 1995. Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron. 15:585-596.
12. Dyer, C.A., and J.M. Matthieu. 1994. Antibodies to myelin/oligodendrocyte-specific protein and myelin/oligodendrocyte glycoprotein signal distinct changes in the organization of cultured oligodendroglial membrane sheets. J. Neurochem. 62:777-787.
13. Dyer, C.A., T.M. Philibotte, M.K. Wolf, and G.S. Billings. 1994. Myelin basic protein mediates extracellular signals that regulate microtubule stability in oligodendrocyte membrane sheets. J. Neurosci. Res. 39:97-107.
14. Ellison, J.A., and V.J. de. 1994. Platelet-derived growth factor receptor is expressed by cells in the early oligodendrocyte lineage. J. Neurosci. Res. 37:116-128.
15. Falls, D.L., K.M. Rosen, G. Corfas, W.S. Lane, and G.D. Fischbach. 1993. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell. 72:801-815.
16. Gallo, V., and R.C. Armstrong. 1995. Developmental and growth factor-induced regulation of nestin in oligodendrocyte lineage cells. J. Neurosci. 15:394-406.
17. Gard, A.L., and S.E. Pfeiffer. 1989. Oligodendrocyte progenitors isolated directly from developing telencephalon at a specific phenotypic stage: myelinogenic potential in a defined environment. Development (Camb.). 106:119-132.
18. - oligodendrocyte progenitors. Dev. Biol. 159:618-630.
19. Goldman, J.E. 1992. Regulation of oligodendrocyte differentiation. Trends Neurosci. 15:359-362.
20. Goodearl, A.D., J.B. Davis, K. Mistry, L. Minghetti, M. Otsu, M.D. Waterfield, and P. Stroobant. 1993. Purification of multiple forms of glial growth factor. J. Biol. Chem. 268:18095-18102.
21. Grinspan, J., L. Wrabetz, and J. Kamholz. 1993. Oligodendrocyte maturation and myelin gene expression in PDGF-treated cultures from rat cerebral white matter. J. Neurocytol. 22:322-333.
22. Grinspan, J.B., and B. Franceschini. 1995. Platelet-derived growth factor is a survival factor for PSA-NCAM+ oligodendrocyte pre-progenitor cells. J. Neurosci. Res. 41:540-551.
23. Grinspan, J.B., J.L. Stern, S.M. Pustilnik, and D. Pleasure. 1990. Cerebral white matter contains PDGF-responsive precursors to O2A cells. J. Neurosci. 10:1866-1873.
24. Grinspan, J.B., M.A. Marchionni, M. Reeves, M. Coulaloglou, and S.S. Scherer. 1996. Axonal interactions regulate Schwann cell apoptosis in the developing peripheral nerve: neuregulin receptors and the role of neuregulins. J. Neurosci. 16:6107-6118.
25. Hart, I.K., W.D. Richardson, C.H. Heldin, B. Westermark, and M.C. Raff. 1989. PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O-2A) cell lineage. Development (Camb.). 105:595-603.
26. Holmes, W.E., M.X. Sliwkowski, R.W. Akita, W.J. Henzel, J. Lee, J.W. Park, D. Yansura, N. Abadi, H. Raab, G.D. Lewis, et al. 1992. Identification of heregulin, a specific activator of p185erbB2. Science (Wash. DC). 256:1205-1210.
27. Huang, C.L., and R.J. Keynes. 1983. Terminal sprouting of mouse motor nerves when the post-synaptic membrane degenerates. Brain Res. 274: 225-229.
28. Jacobsen, N.E., N. Abadi, M.X. Sliwkowski, D. Reilly, N.J. Skelton, and W.J. Fairbrother. 1996. High-resolution solution structure of the EGF-like domain of heregulin-alpha. Biochemistry. 35:3402-3417.
29. Kita, Y.A., J. Barff, Y. Luo, D. Wen, D. Brankow, S. Hu, N. Liu, S.A. Prigent, W.J. Gullick, and M. Nicolson. 1994. NDF/heregulin stimulates the phosphorylation of Her3/erbB3. FEBS (Fed. Exp. Biol. Soc.) Lett. 349: 139-143.
30. Kleitman, N., P.W. Wood, and R.P. Bunge. 1994. Culturing Nerve Cells. Gary Banker and Kimberly Goslin, editors. MIT Press, Cambridge, MA. 337-377.
31. Kostyk, S.K., P.A. D'Amore, I.M. Herman, and J.A. Wagner. 1994. Optic nerve injury alters basic fibroblast growth factor localization in the retina and optic tract. J. Neurosci. 14:1441-1449.
32. Kraus, M.H., W. Issing, T. Miki, N.C. Popescu, and S.A. Aaronson. 1989. Isolation and characterization of ERBB3, a third member of the ERBB/ epidermal growth factor receptor family: evidence for overexpression in a subset of human mammary tumors. Proc. Natl. Acad. Sci. USA. 86: 9193-9197.
33. Langford, L.A., S. Porter, and R.P. Bunge. 1988. Immortalized rat Schwann cells produce tumours in vivo. J. Neurocytol. 17:521-529.
34. Lemke, G.E. and J.P. Brockes. 1984. Identification and purification of glial growth factor. J. Neurosci. 4:75-83.
35. Levi, A.D., R.P. Bunge, J.A. Lofgren, L. Meima, F. Hefti, K. Nikolics, and M.X. Sliwkowski. 1995. The influence of heregulins on human Schwann cell proliferation. J. Neurosci. 15:1329-1340.
36. Loeb, J.A., and G.D. Fischbach. 1995. ARIA can be released from extra-cellular matrix through cleavage of a heparin-binding domain. J. Cell Biol. 130:127-135.
37. Louis, J.C., E. Magal, D. Muir, M. Manthorpe, and S. Varon. 1992. CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J. Neurosci. Res. 31:193-204.
38. Louis, J.C., E. Magal, S. Takayama, and S. Varon. 1993. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science (Wash. DC). 259:689-692.
39. Ma, J., S.X. Yang, G.J. Ho, and B.W. Festoff. 1994. Insulin-like growth factor binding protein-1 is pre-synaptic at mouse neuromuscular synapses and is transported in nerve. Neurochem. Res. 19:1363-1368.
40. Marchionni, M.A., A.D. Goodearl, M.S. Chen, M.O. Bermingham, C. Kirk, M. Hendricks, F. Danehy, D. Misumi, J. Sudhalter, K. Kobayashi, et al. 1993. Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature (Lond.). 362:312-318.
41. McKinnon, R.D., G. Piras, J.J. Ida, and D.M. Dubois. 1993. A role for TGF-β in oligodendrocyte differentiation. J. Cell Biol. 121:1397-1407.
42. McKinnon, R.D., C. Smith, T. Behar, T. Smith, and D.M. Dubois. 1993. Distinct effects of bFGF and PDGF on oligodendrocyte progenitor cells. Glia. 7:245-254.
43. McMorris, F.A., and D.M. Dubois. 1988. Insulin-like growth factor I promotes cell proliferation and oligodendroglial commitment in rat glial progenitor cells developing in vitro. J. Neurosci. Res. 21:199-209.
44. McMorris, F.A., R.W. Furlanetto, R.L. Mozell, M.J. Carson, and D.W. Raible. 1990. Regulation of oligodendrocyte development by insulin-like growth factors and cyclic nucleotides. Ann. NY Acad. Sci. 605:101-109.
45. McMorris, F.A., R.L. Mozell, M.J. Carson, Y. Shinar, R.D. Meyer, and N. Marchetti. 1993. Regulation of oligodendrocyte development and central nervous system myelination by insulin-like growth factors. Ann. NY Acad. Sci. 692:321-334.
46. Meyer, D., and C. Birchmeier. 1995. Multiple essential functions of neuregulin in development. Nature (Lond.). 378:386-390.
47. Morrissey, T.K., A.D. Levi, A. Nuijens, M.X. Sliwkowski, and R.P. Bunge. 1995. Axon-induced mitogenesis of human Schwann cells involves heregulin and p185erbB2. Proc. Natl. Acad. Sci. USA. 92:1431-1435.
48. Mudhar, H.S., R.A. Pollock, C. Wang, C.D. Stiles, and W.D. Richardson. 1993. PDGF and its receptors in the developing rodent retina and optic nerve. Development (Camb.). 118:539-552.
49. Nieto, B.M., S.L. Garcia, and A.I. Torres. 1993. Orthograde transport and release of insulin-like growth factor I from the inferior olive to the cerebellum. J. Neurosci. Res. 36:520-527.
50. Nishio, T., S. Furukawa, I. Akiguchi, N. Oka, K. Ohnishi, H. Tomimoto, S. Nakamura, and J. Kimura. 1994. Cellular localization of nerve growth factor-like immunoreactivity in adult rat brain: quantitative and immunohistochemical study. Neuroscience. 60:67-84.
51. Noll, E., and R.H. Miller. 1994. Regulation of oligodendrocyte differentiation: a role for retinoic acid in the spinal cord. Development (Camb.). 120:649-660.
52. Orr, U.A., L. Trakhtenbrot, L.R. Ben, D. Wen, G. Rechavi, P. Lonai, and Y. Yarden. 1993. Neural expression and chromosomal mapping of Neu differentiation factor to 8p12-p21. Proc. Natl. Acad. Sci. USA. 90:1867-1871.
53. Peles, E., and Y. Yarden. 1993. Neu and its ligands: from an oncogene to neural factors. BioEssays. 15:815-824.
54. Peles, E., L.R. Ben, E. Tzahar, N. Liu, D. Wen, and Y. Yarden. 1993. Cell-type specific interaction of Neu differentiation factor (NDF/heregulin) with Neu/HER-2 suggests complex ligand-receptor relationships. EMBO (Eur. Mol. Biol. Organ.) J. 12:961-971.
55. Plowman, G.D., J.M. Culouscou, G.S. Whitney, J.M. Green, G.W. Carlton, L. Foy, M.G. Neubauer, and M. Shoyab. 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.
56. Porter, S., L. Glaser, and R.P. Bunge. 1987. Release of autocrine growth factor by primary and immortalized Schwann cells. Proc. Natl. Acad. Sci. USA. 84:7768-7772.
57. Qian, X., C.M. LeVea, J.K. Freeman, W.C. Dougall, and M.I. Greene. 1994. Heterodimerization of epidermal growth factor receptor and wild-type or kinase-deficient Neu: a mechanism of interreceptor kinase activation and transphosphorylation. Proc. Natl. Acad. of Sci. USA. 91:1500-1504.
58. Quiroga, S., R.S. Garofalo, and K.H. Pfenninger. 1995. Insulin-like growth factor I receptors of fetal brain are enriched in nerve growth cones and contain a β-subunit variant. Proc. Natl. Acad. Sci. USA. 92:4309-4312.
59. Raff, M.C., E. Abney, J.P. Brockes, and A. Hornby-Smith. 1978. Schwann cell growth factors. Cell. 15:813-822.
60. Raff, M.C., R.H. Miller, and M. Noble. 1983. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature (Lond.). 303:390-396.
61. Raff, M.C., L.E. Lillien, W.D. Richardson, J.F. Burne, and M.D. Noble. 1988. Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture. Nature (Lond.). 333:562-565.
62. Ratner, N., P. Wood, L. Glaser, and R.P. Bunge. 1987. Further characterization of the neuronal cell surface protein mitogenic for Schwann cells. In Glial-Neuronal Communication in Development and Regeneration. H.H. Althaus and W. Seifert, editors. Springer-Verlag, Heidelberg. 685-697.
63. Salzer, J.L., and R.P. Bunge. 1980. Studies of Schwann cell proliferation I. An analysis in tissue culture of proliferation during development, Wallerian degeneration, and direct injury. J. Cell Biol. 84:739-752.
64. Sandrock, A.J., A.D. Goodearl, Q.W. Yin, D. Chang, and G.D. Fischbach. 1995. ARIA is concentrated in nerve terminals at neuromuscular junctions and at other synapses. J. Neurosci. 15:6124-6136.
65. Schecterson, L.C., and M. Bothwell. 1992. Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron. 9:449-463.
66. Shah, N.M., M.A. Marchionni, I. Isaacs, P. Stroobant, and D.J. Anderson. 1994. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell. 77:349-360.
67. Sliwkowski, M.X., G. Schaefer, R.W. Akita, J.A. Lofgren, V.D. Fitzpatrick, A. Nuijens, B.M. Fendly, R.A. Cerione, R.L. Vandlen, and K.L. Carraway III. 1994. Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin. J. Biol. Chem. 269:14661-14665.
68. Torriglia, A., J.C. Jeanny, and P.R. Blanquet. 1994. Immunohistochemical analysis of fibroblast growth factor receptor in bovine retina. Neurosci. Lett. 172:125-128.
69. Vartanian, T., G. Corfas, Y. Li, G.D. Fischbach, and K. Stefansson. 1994. A role for the acetylcholine receptor-inducing protein ARIA in oligodendrocyte development. Proc. Natl. Acad. Sci. USA. 91:11626-11630.
70. Wallasch, C., F.U. Weiss, G. Niederfellner, B. Jallal, W. Issing, and A. Ullrich. 1995. Heregulin-dependent regulation of HER2/neu oncogenic signaling by heterodimerization with HER3. EMBO (Eur. Mol. Biol. Organ.) J. 14:4267-4275.
71. Wen, D., E. Peles, R. Cupples, S.V. Suggs, S.S. Bacus, Y. Luo, G. Trail, S. Hu, S.M. Silbiger, R.B. Levy, et al. 1992. Neu differentiation factor: a transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell. 69:559-572.
72. Wen, D., S.V. Suggs, D. Karunagaran, N. Liu, R.L. Cupples, Y. Luo, A.M. Janssen, B.N. Ben, D.B. Trollinger, V.L. Jacobsen, et al. 1994. Structural and functional aspects of the multiplicity of Neu differentiation factors. Mol. Cell. Biol. 14:1909-1919.
73. Wolswijk, G., and M. Noble. 1992. Cooperation between PDGF and FGF converts slowly dividing O-2A adult progenitor cells to rapidly dividing cells with characteristics of O-2A perinatal progenitor cells. J. Cell Biol. 118:889-900.
74. Wood, P., and R.P. Bunge. 1975. Evidence that sensory axons are mitogenic for Schwann cells. Nature (Lond.). 256:662-664.