Vestibular Schwann Cells Are a Distinct Subpopulation of Peripheral Glia with Specific Sensitivity to Growth Factors and Extracellular Matrix Components

Journal of Neurobiology

Volumn 57, Issue 3, 2003, Pages 270-290

  Bartolami, Sylvain ^a   Augé, Christelle ^a   Travo, Cécile ^a   Ventéo, Stéphanie ^a   Knipper, Marlies ^b   Sans, Alain ^a  

^a INSERM   (France)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Extracellular matrix proteins; Growth factors; Inner ear; NF2 type 2 neurofibromatosis protein; Phenotype; Proliferation; Vestibular Schwann cells

Indexed keywords

BROXURIDINE; FIBROBLAST GROWTH FACTOR 2; FIBRONECTIN; FORSKOLIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; LYSINE; MESSENGER RNA; MITOGENIC AGENT; MYELIN BASIC PROTEIN; PROGESTERONE; SOMATOMEDIN BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DENSITY; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; EVALUATION; EXTRACELLULAR MATRIX; GLIA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCHWANN CELL; VESTIBULAR NERVE;

ANIMALS; CELL COUNT; CELL DIVISION; CELL SURVIVAL; CELLS, CULTURED; EXTRACELLULAR MATRIX PROTEINS; GROWTH SUBSTANCES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; RATS; SCHWANN CELLS; SCIATIC NERVE; VESTIBULAR NERVE;

EID: 0242721446     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10302     Document Type: Article

References (72)

1. Baron van Evercooren A, Gansmüller A, Gumpel M, Baumann N, Kleinman HK. 1986. Schwann cell differentiation in vitro: extracellular matrix deposition and interaction and motility. J Cell Biol 93:211-216.
2. Bermingham-McDonogh O, Xu YT, Marchionni MA, Scherer SS. 1997. Neuregulin expression in PNS neurons: isoforms and regulation by target interactions. Mol Cell Neurosci 10:184-195.
3. Bianchini D, De Martini I, Cadoni A, Zicca A, Tabaton M, Schenone A, Anfosso S, Akkad Wattar AS, Zaccheo D, Mancardi GL. 1992. GFAP expression of human Schwann cells in tissue culture. Brain Res 570:209-217.
4. Campana WM, Darin SJ, O'Brien JS. 1999. Phosphatidylinositol 3-kinase and Akt protein kinase mediate IGF-1 and prosamide-induced survival in Schwann cells. J Neurosci Res 57:332-341.
5. Canoll PD, Kraemer R, Teng KK, Marchionni MA, Salzer JL. 1999. GGF/Neuregulin induces a phenotypic reversion of oligodendrocytes. Mol Cell Neurosci 13:79-94.
6. Chan RJ, Cosgaya JM, Wu YJ, Shooter EM. 2001. Neurotrophins are key mediators of the myelination program in the peripheral nervous system. Proc Natl Acad Sci USA 98:14661-14668.
7. Chausovsky A, Waterman H, Elbaum M, Yarden Y, Geiger B, Bershadsky AD. 2000. Molecular requirements for the effect of neuregulin on cell spreading, motility and colony organization. Oncogene 19:878-888.
8. Chuah MI, Cossins JM, Woodhall E, Tennent R, Nash G, West AK. 2000. Glial growth factor 2 induces proliferation and structural changes in ensheathing cells. Brain Res 857:265-274.
9. D'Amico-Martel A, Noden DM. 1983. Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am J Anat 166:445-468.
10. Dashiell SM, Koski CL. 1999. Sublytic terminal complement complexes decrease PO gene expression in Schwann cells. J Neurochem 73:2321-2330.
11. Dong Z, Dean C, Walters JE, Mirsky R, Jessen KR. 1997. Response of Schwann cells to mitogen in vitro is determined by pre-exposure to serum, time in vitro and developmental age. Glia 20:219-230.
12. Eccleston PA, Collarini EJ, Jessen KR, Mirsky R, Richardson WD. 1990. Schwann cells secrete a PDGF-like factor: evidence for an autocrine growth mechanism involving PDGF. Eur J Neurosci 2:985-992.
13. Evans DGR, Sainio M, Baser ME. 2000. Neurofibromatosis type 2. J Med Genet 37:897-904.
14. Fernandez Valle C, Bunge RP, Bunge MB. 1995. Schwann cells degrade myelin and proliferate in the absence of macrophages: evidence from in vitro studies of Wallerian degeneration. J Neurocytol 24:667-679.
15. Fernandez Valle C, Gorman D, Gomez AM, Bunge MB. 1997. Actin plays a role in both changes in cell shape and gene-expression associated with Schwann cell myelination. J Neurosci 17:241-250.
16. Franceschini IA, Barnett SC. 1996. Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev Biol 173:327-343.
17. Fu SY, Gordon T. 1997. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol 14:67-116.
18. Funakoshi H, Frisen J, Barbany G, Timmusk T, Zachrisson O, Verge VMK, Persson H. 1993. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123:455-465.
19. Goda S, Hammer J, Kobiler D, Quarles RH. 1991. Expression of the myelin-associated glycoprotein in cultures of immortalized Schwann cells. J Neurochem 56:1354-1361.
20. Hammarberg H, Piehl F, Cullheim S, Fjell J, Hökfelt T, Fried K. 1996. GDNF mRNA in Schwann cells and DRG satellite cells after chronic sciatic nerve injury. NeuroReport 7:857-860.
21. Hammarberg H, Risling M, Hökfelt T, Cullheim S, Piehl F. 1998. Expression of insulin-like growth factors and corresponding binding proteins (IGFBP 1-6) in rat spinal cord and peripheral nerve after axonal injuries. J Comp Neurol 400:57-72.
22. Hansen MR, Vijapurkar U, Koland JG, Green SH. 2001. Reciprocal signaling between spiral ganglion neurons and Schwann cells involves neuregulin and neurotrophins. Hear Res 161:87-98.
23. Henderson CE, Phillips HS, Pollock RA, Davies AM, Lemeulle C, Armanini M, Simpson LC, Moffet B, Vandlen RA, Koliatsos VE, et al. 1994. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266:1062-1064.
24. Hijazi MM, Thompson EW, Tang C, Coopman P, Torri JA, Yang D, Mueller SC, Lupu R. 2000. Heregulin regulates the actin cytoskeleton and promotes invasive properties in breast cancer cell lines. Int J Oncology 17:629-641.
25. Ho WH, Armanini, MP, Nuijens A, Phillips HS, Osheroff PL. 1995. Sensory and motor neuron-derived factor, a novel heregulin variant highly expressed in sensory and motor neurons. J Biol Chem 270:14523-14532.
26. Höke A, Gordon T, Zochodne DW, Sulaiman OAR. 2002. A decline in glial cell-line-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp Neurol 173:77-85.
27. Höke A, Ho T, Crawford TO, Lebel C, Hilt D, Griffin JW. 2003. Glial cell line derived neurotrophique factor alters axon Schwann cell unit and promotes myelination in unmyelinated fibers. J Neurosci 23:561-567.
28. Jessen KR, Brennan A, Morgan L, Mirsky R, Kent A, Hashimoto Y, Gavrilovic J. 1994. The Schwann cell precursor and its fate: a study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron 12:509-527.
29. Jessen KR, Mirsky R. 1991. Schwann cell precursors and their development. Glia 4:185-194.
30. Jessen KR, Mirsky R. 1999. Schwann cell and their precursors emerge as major regulators of nerve development. Trends Neurosci 22:402-410.
31. Jessen KR, Morgan L, Mirsky R. 1987. Myelinated, but not unmyelinated reversibly down-regulate N-CAM in Schwann cells. J Neurocytol 16:681-688.
32. Jessen KR, Morgan L, Stewart HJS, Mirsky R. 1990. Three markers of adult non-myelin-forming Schwann cells, 217c (Ran-1) A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions. Development 109:91-103
33. Kim SU, Yong VW, Watabe K, Shin DH. 1989. Human fetal Schwann cells in culture: phenotypic expression and proliferative capability. J Neurosci Res 22:50-59.
34. Kioussi C, Gross MK, Gruss P. 1995. Pax3: a paired domain gene as a regulateur in PNS myelination. Neuron 15:553-562.
35. Kursula P, Lehto VP, Heape AM. 2001. The small myelin-associated glycoprotein binds tubulin and microtubules. Mol Brain Res 87:22-30.
36. Lemke G. 1993. The molecular genetics of myelination - an update. Glia 7:263-271.
37. Lemke G, Chao M. 1988. Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development 102:499-504.
38. Lobsiger CS, Schweitzer B, Taylor V, Suter U. 2000. Platelet-derived growth factor-BB supports the survival of cultured rat Schwann cell precursor in synergy with neurotrophin-3. Glia 30:290-300.
39. Lobsiger CS, Smith PM, Buchstaller J, Schweitzer B, Franklin RJM, Suter U, Taylor V. 2001. SpL201: a conditionally immortalized Schwann cell precursor line that generates myelin. Glia 36:31-47.
40. Love FM, Thompson WJ. 1998. Schwann cells proliferate at rat neuromuscular junction during development and regeneration. J Neurosci 18:9376-9385.
41. Marchionni MA, Goodearl ADJ, Chen MS, Bermingham-McDonogh O, Kirk C, Hendricks M, Danehy F, Misumi D, Sudhalter J, Kobayashi K, et al. 1993. Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362:312-318.
42. Martini R. 2001. The effect of myelinating Schwann cells on axons. Muscle Nerve 24:456-466.
43. Mata M, Alessi D, Fink DJ. 1990. S100 is preferentially distributed in myelin-forming Schwann cells. J Neurocytol 19:432-442.
44. Meier C, Parmentier E, Brennan A, Mirsky R, Jessen KR. 1999. Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving IGF, NT-3 and PDGF-BB. J Neurosci 19:3847-3859.
45. Mirsky R, Jessen KR. 1996. Schwann cell development, differentiation and myelination. Curr Opin Neurobiol 6:89-96.
46. Mokuno K, Kamholtz J, Behrman T, Black C, Sessa M, Feinstein D, Lee V, Pleasure D. 1989. Neuronal modulation of Schwann cell glial fibrillary acidic protein (GFAP). J Neurosci Res 23:396-405.
47. Pixley SK. 1992. The olfactory nerve contains two populations of glia, identified both in vivo and in vitro. Glia 5:269-284
48. Podratz JL, Rodriguez E, Windebank AJ. 2001. Role of the extracellular matrix in myelination of peripheral nerve. Glia 35:35-40.
49. Porter S, Clark MB, Glaser L, Bunge RP. 1986. Schwann cells stimulated to proliferate in the absence of neurons retain full functional capability. J Neurosci 6:3070-3078.
50. Raabe TD, Clive DR, Neuberger TJ, Wen D, De Vries GH. 1996. Cultured neonatal Schwann cells contains and secrete neuregulins. J Neurosci Res 46:263-270.
51. Rosenbaum C, Karyala S, Marchionni MA, Kim HA, Krasnoselsky AL, Happel B, Isaacs I, Brackenburry R, Ratner N. 1997. Schwann cells express NDF and SMDF/nARIA mRNAs, secrete neuregulin and show constitutive activation of erbB3 receptors: evidence for a neuregulin autocrine loop. Exp Neurol 148:604-615.
52. Rouleau GA, Merel P, Lutchman M, Sanson M, Zucman J, Marineau C, Hoang-Xuan K, Demczuk S, Desmaze C, Plougastel B, et al. 1993. alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature 363:515-521.
53. Sans A, Bartolami S, Fraysse B. 1996. Histopathology of the peripheral vestibular system in small vestibular schwannomas. Am J Otology 17:326-334.
54. Shah NM, Marchionni MA, Issac I, Stroobant P, Anderson DJ. 1994. Glial growth factor restricts mammalian neural crest stem cells to glial fate. Cell 77:349-360.
55. Sherman LS, Gutmann DH. 2001. Merlin: hanging tumor suppression on the Rac. Trends Cell Biol 11:442-444.
56. Son YJ, Trachtenberg JT, Thompson WJ. 1996. Schwann cells induce and guide spouting and reinnervation of neuromuscular junctions. Trends Neurosci 19:280-285.
57. Stewart HJS, Morgan L, Jessen KR, Mirsky R. 1993. Changes in DNA synthesis rate in the Schwann cell lineage in vivo are correlated with the precursor-Schwann cell transition and myelination. Eur J Neurosci 5:1136-1144.
58. 3H]thymidine incorporation through their respective receptors. Glia 18:68-72.
59. Syroid DE, Zorick TS, Arbet-Engels C, Kilpatrick TJ, Eckhart W, Lemke G. 1999. A role for insulin-like growth factor-1 in the regulation of Schwann cell survival. J Neurosci 19:2059-2068.
60. Tohyama K, Ide C. 1984. The localization of laminin and fibronectin on the Schwann cell basal lamina. Arch Histol Jap 47:519-532.
61. Topilko P, Levi G, Merlo G, Mantero S, Desmarquet C, Mancardi G, Charnay P. 1997. Differential regulation of the zinc finger genes Krox-20 and Krox-24 (Egr-1) suggests antagonistic roles in Schwann cells. J Neurosci Res 50:702-712.
62. Trachtenberg JT, Thompson WJ. 1996. Schwann cell apoptosis at developing neuromuscular junction is regulated by glial growth factor. Nature 379:174-177.
63. Trofatter JA, MacCollin MM, Rutter JL, Murrell JR, Duyao MP, Parry DM, Eldridge R, Kley N, Menon AG, Pulaski K, et al. 1993. A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 72:791-800.
64. Tsiper MV, Yurchenco PD. 2002. Laminin assembles into separate basement membrane and fibrillar matrices in Schwann cells. J Cell Sci 115:1005-1015.
65. Verdi JM, Groves AK, Farinas I, Jones K, Marchionni MA, Reichardt LF, Anderson DJ. 1996. A reciprocal cell-cell interaction mediated by NT-3 and neuregulin controls the early survival and development of sympathetic neuroblasts. Neuron 16:515-527.
66. Vincent AJ, West AK, Chuah MI. 2003. Morphological plasticity of olfactory ensheathing cells is regulated by cAMP and endothelin-1. Glia 41:393-403.
67. Watabe K, Fukuda T, Tanaka J, Honda H, Toyohara K, Sakai O. 1995. Spontaneously immortalized adult mouse Schwann cells secrete autocrine and paracrine growth-promoting activities. J Neurosci Res 41:279-290.
68. Weiner JA, Fukushima N, Contos JJA, Scherer SS, Chun J. 2001. Regulation of Schwann cell morphology and adhesion by receptor-mediated lysophosphatidic acid signaling. J Neurosci 21:7069-7078.
69. Wood PM, Schachner M, Bunge RP. 1990. Inhibition of Schwann cell myelination in vitro by antibody to the L1 adhesion molecule. J Neurosci 10:3635-3645.
70. Yin X, Crawford TO, Griffin JW, Tu PH, Lee VMY, Li C, Roder J, Trapp BD. 1998. Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J Neurosci 18:1953-1962.
71. Zanazzi G, Einheber S, Westreich R, Hannocks MJ, Bedell-Hogan D, Marchionni MA, Salzer J. 2001. Glial growth factor/neuregulin inhibits Schwann cell myelination and induces demyelination. J Cell Biol 152:1289-1299.
72. Zorick TS, Lemke G. 1996. Schwann cell differentiation. Curr Opin Cell Biol 8:870-876.