Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth

Journal of Neuroscience

Volumn 16, Issue 15, 1996, Pages 4673-4683

  Mahanthappa, Nagesh K ^a,c   Anton, Eva S ^b,d   Matthew, William D ^b  

^a CeNeS Pharmaceuticals plc   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c Ontogeny Inc   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

glial growth factor; migration; nerve regeneration; neuregulin; neurotrophic activity; Schwann cell

Indexed keywords

NEURITE PROMOTING FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; MOTONEURON; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SCHWANN CELL;

EID: 0029896428     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-15-04673.1996     Document Type: Article

References (42)

1. Anton ES, Weskamp G, Reichardt LF, Matthew WD (1994) Nerve growth factor and its low affinity receptor promote Schwann cell migration. Proc Natl Acad Sci USA 91:2795-2799.
2. Banerjee A, Roach MC, Trcka P, Luduena RF (1990) Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of β-tubulin. J Biol Chem 1990:1794-1799.
3. Brockes JP (1987) Assay and isolation of glial growth factor from the bovine pituitary. Methods Enzymol 147:217-225.
4. Carraway KL, Burden SJ (1995) Neuregulins and their receptors. Curr Biol 5:1-7.
5. Chen MS, Bermingham-McDonogh O, Danehy FT, Nolan C, Scherer SS, Lucas J, Gwynne D, Marchionni MA (1994) Expression of multiple neuregulin transcripts in postnatal rat brains. J Comp Neurol 349:389-400.
6. Cohen JA, Yachnis AT, Arai M, Davis JG, Scherer SS (1992) Expression of the neu proto-oncogene by Schwann cells during peripheral nerve development and Wallerian degeneration. J Neurosci Res 31:622-634.
7. Curtis R, Scherer SS, Somogyi R, Adryan KM, Ip NY, Zhu Y, Lindsay RM, DiStefano PS (1994) Retrograde axonal transport of LIF is increased by peripheral nerve injury: correlation with increased LIF expression in the distal nerve. Neuron 12:191-204.
8. Dong Z, Brennan A, Liu N, Yarden Y, Lefkowitz G, Mirsky 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.
9. ElShamy WM, Linnarsson S, Lee K-F, Jaenisch R, Ernfors P (1996) Prenatal and postnatal requirements of NT-3 for sympathetic neuroblast survival and innervation of specific targets. Development 122:491-500.
10. 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.
11. Friedman B, Scherer SS, Rudge JS, Helgren M, Morrisey D, McClain J, Wang D, Furth ME, Lindsay RM, Ip NY (1992) Regulation of ciliary neurotrophic factor expression in myelin-related Schwann cells in vivo. Neuron 9:295-305.
12. Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R, Lemke G (1995) Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378:390-394.
13. Goodearl ADJ, Davis JB, Mistry K, Minghetti L, Otsu M, Waterfield MD, Stroobant P (1993) Purification of multiple forms of glial growth factor. J Biol Chem 268:18095-18102.
14. Gunderson RW, Barrett JN (1980) Characterization of the turning response of dorsal root neurites toward nerve growth factor. J Cell Biol 87:546-554.
15. erbB2. Science 256:1205-1210.
16. Jessen KR, Mirsky R (1992) Schwann cells: early lineage, regulation of proliferation and control of myelin formation. Curr Opin Neurobiol 2:575-581.
17. Jin JJ, Nikitin AY, Rajewsky MF (1993) Schwann cell lineage-specific neu (erbB-2) gene expression in the developing rat nervous system. Cell Growth Differ 4:227-237.
18. Kuffler DP (1986) Isolated satellite cells of a peripheral nerve direct the growth of regenerating frog axons. J Comp Neurol 249:57-64.
19. LeBeau JM, LaCorbiere M, Powell HC, Ellisman MH, Schubert D (1988) Extracellular fluid conditioned during peripheral nerve regeneration stimulates Schwann cell adhesion, migration, and proliferation. Brain Res 459:93-104.
20. Lee K-F, Simon H, Chen H, Bates B, Hung M-C, Hauser C (1995) Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378:394-398.
21. Lemke GE, Brockes JP (1984) Identification and purification of glial growth factor. J Neurosci 4:75-83.
22. Marchionni MA, Goodearl ADJ, Chen MS, Bermingham-McDonogh O, Kirk C, Henricks 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.
23. Martini R, Schachner M, Faissner A (1990) Enhanced expression of the extracellular matrix molecule J1/tenascin in the regenerating adult mouse sciatic nerve. J Neurocytol 19:601-616.
24. Meyer D, Birchmeier C (1994) Distinct isoforms of neuregulin are expressed in mesenchymal and neuronal cells during mouse development. Proc Natl Acad Sci USA 91:1064-1068.
25. Meyer D, Birchmeier C (1995) Multiple essential functions of neuregulin in development. Nature 378:386-390.
26. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H (1992) Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol 119:45-54.
27. erbB2 are involved in axon-induced Schwann cell proliferation. Soc Neurosci Abstr 20:707.
28. Mudge AW (1993) New ligands for Neu? Curr Biol 3:361-364.
29. Orr-Urtreger A, Trakhtenbrot L, Ben-Levy R, Wen D, Rechavi G, Lonai P, Yarden Y (1993) Neural expression and chromosomal mapping of Neu differentiation factor to 8p12-p21. Proc Natl Acad Sci USA 90:1867-1871.
30. Patterson PH (1985) On the role of proteases, their inhibitors, and the extracellular matrix in promoting neurite outgrowth. J Physiol (Paris) 80:207-211.
31. Peles E, Yarden Y (1993) Neu and its ligands: from an oncogene to neural factors. Bioessays 15:815-824.
32. Politis MJ, Ederle K, Spencer PS (1982) Tropism in nerve regeneration in vivo. Attraction of regenerating axons by diffusible factors derived from cells in distal nerve stumps of transected peripheral nerves. Brain Res 253:1-12.
33. Ramon y Cajal S (1928) Degeneration and regeneration of the nervous system. Oxford: Oxford UP.
34. Reichardt LF, Tomaselli KJ (1991) Extracellular matrix molecules and their receptors: functions in neural development. Annu Rev Neurosci 14:531-570.
35. Rutkowski JL, Kirk CJ, Lerner MA, Tennekoon GI (1995) Purification and expression of human Schwann cells in vitro. Nature Med 1:80-83.
36. Salzer JL, Bunge RP, Glaser L (1980a) Studies of Schwann cell proliferation. III. Evidence for the surface localization of then neurite mitogen. J Cell Biol 84:767-778.
37. Salzer JL, Williams AK, Glaser L, Bunge RP (1980b) Studies of Schwann cell proliferation. II. Characterization of the stimulation and specificity of the response to a neurite membrane fraction. J Cell Biol 84:753-766.
38. Scherer SS, Salzer JL (1996) Axon-Schwann cell interactions during peripheral nerve degeneration and regeneration. In: Glial cell development: basic principles and clinical relevance (Jessen KR, Richardson WD, eds). Oxford: Bios Scientific.
39. Shah NM, Marchionni MA, Issacs I, Stoobant P, Anderson DJ (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77:349-360.
40. Sudhalter J, Whitehouse L, Rusche JR, Marchionni MA, Mahanthappa NK (1996) Schwann cell heparan sulfate proteoglycans play a critical role in glial growth factor/neuregulin signaling. Glia 17:28-38.
41. Trachtenberg JT, Thompson WJ (1996) Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379:174-177.
42. Wen D, Peles E, Cupples R, Suggs SV, Bacus SS, Luo Y, Trail G, Hu S, Silberger SM, Ben-Levy R, Koski RA, Lu HS, Yarden Y (1992) Neu differentiation factor: a transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell 69:559-572.