Neural cell adhesion molecule stimulates survival of premyelinating oligodendrocytes via the fibroblast growth factor receptor

Journal of Neuroscience Research

Volumn 87, Issue 15, 2009, Pages 3356-3368

  Palser, Anne L ^a   Norman, Adele L ^a   Saffell, Jane L ^a   Reynolds, Richard ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Cell signalling; Myelination; NCAM; Oligodendrocyte

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR; FIBRONECTIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NERVE CELL ADHESION MOLECULE;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; IN VITRO STUDY; MONOLAYER CULTURE; MOUSE; MYELINATION; NERVE CELL STIMULATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL SHAPE; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; MAP KINASE SIGNALING SYSTEM; MICE; MYELIN SHEATH; NEURAL CELL ADHESION MOLECULES; NIH 3T3 CELLS; OLIGODENDROGLIA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, FIBROBLAST GROWTH FACTOR; STEM CELLS;

EID: 70449346696     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22248     Document Type: Article

References (51)

1. Anderson AA, Kendal CE, Garcia-Maya M, Kenny AV, Morris-Triggs SA, Wu T, Reynolds R, Hohenester E, Saffell JL. 2005. A peptide from the first fibronectin domain of NCAM acts as an inverse agonist and stimulates FGF receptor activation, neurite outgrowth and survival. J Neurochem 95:570-583. (Pubitemid 41457525)
2. Bansal R, Kumar M, Murray K, Morrison RS, Pfeiffer SE. 1996. Regulation of FGF receptors in the oligodendrocyte lineage. Mol Cell Neurosci 7:263-275. (Pubitemid 26187836)
3. Bansal R, Magge S, Winkler S. 2003. Specific inhibitor of FGF receptor signaling: FGF-2-mediated effects on proliferation, differentiation, and MAPK activation are inhibited by PD173074 in oligodendrocyte-line-age cells. J Neurosci Res 74:486-493. (Pubitemid 37352070)
4. Baron W, Colognato H, ffrench-Constant C. 2005. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia 49:467-479.
5. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, Raff MC. 1992. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70:31-46.
6. Barres BA, Jacobson MD, Schmid R, Sendtner M, Raff MC. 1993. Does oligodendrocyte survival depend on axons? Curr Biol 3:489-497.
7. Bartsch U, Kirchhoff F, Schachner M. 1990. Highly sialylated N-CAM is expressed in adult mouse optic nerve and retina. J Neurocytol 19:550-565. (Pubitemid 20263995)
8. Bhat S, Silberberg DH. 1986. Oligodendrocyte cell adhesion molecules are related to neural cell adhesion molecule (N-CAM). J Neurosci 6: 3348-3354. (Pubitemid 17186060)
9. Bhat S, Silberberg DH. 1988. Developmental expression of neural cell adhesion molecules of oligodendrocytes in vivo and in culture. J Neurochem 50:1830-1838. (Pubitemid 18140740)
10. Burne JF, Staple JK, Raff MC. 1996. Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons. J Neurosci 16:2064-2073.
11. Cambon K, Hansen SM, Venero C, Herrero AI, Skibo G, Berezin V, Bock E, Sandi C. 2004. A synthetic neural cell adhesion molecule mimetic peptide promotes synaptogenesis, enhances presynaptic function, and facilitates memory consolidation. J Neurosci 24:4197-4204. (Pubitemid 38620795)
12. Carafoli F, Saffell JL, Hohenester E. 2008. Structure of the tandem fibronectin type 3 domains of neural cell adhesion molecule. J Mol Biol 377:524-534.
13. Charles P, Hernandez MP, Stankoff B, Aigrot MS, Colin C, Rougon G, Zalc B, Lubetzki C. 2000. Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc Natl Acad Sci U S A 97:7585-7590. (Pubitemid 30431507)
14. Charles P, Reynolds R, Seilhean D, Rougon G, Aigrot MS, Niezgoda A, Zalc B, Lubetzki C. 2002. Re-expression of PSA-NCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis? Brain 125:1972-1979.
15. Colognato H, Baron W, Vellana-Adalid V, Relvas JB, Baron-Van EA, Georges-Labouesse E, ffrench-Constant C. 2002. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat Cell Biol 4:833-841.
16. Colognato H, Ramachandrappa S, Olsen IM, ffrench-Constant C. 2004. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J Cell Biol 167:365-375.
17. David S, Miller RH, Patel R, Raff MC. 1984. Effects of neonatal transection on glial cell development in the rat optic nerve: evidence that the oligodendrocyte-type 2 astrocyte cell lineage depends on axons for its survival. J Neurocytol 13:961-974. (Pubitemid 15167231)
18. Doherty P, Barton CH, Dickson G, Seaton P, Rowett LH, Moore SE, Gower HJ, Walsh FS. 1989. Neuronal process outgrowth of human sensory neurons on monolayers of cells transfected with cDNAs for five human N-CAM isoforms. J Cell Biol 109:789-798. (Pubitemid 19197037)
19. Doherty P, Fruns M, Seaton P, Dickson G, Barton CH, Sears TA, Walsh FS. 1990. A threshold effect of the major isoforms of NCAM on neurite outgrowth. Nature 343:464-466. (Pubitemid 20065233)
20. Doherty P, Rowett LH, Moore SE, Mann DA, Walsh FS. 1991. Neurite outgrowth in response to transfected N-CAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs. Neuron 6:247-258.
21. Edelman GM, Chuong CM. 1982. Embryonic to adult conversion of neural cell adhesion molecules in normal and staggerer mice. Proc Natl Acad Sci U S A 79:7036-7040.
22. Fernandez PA, Tang DG, Cheng L, Prochiantz A, Mudge AW, Raff MC. 2000. Evidence that axon-derived neuregulin promotes oligodendrocyte survival in the developing rat optic nerve. Neuron 28:81-90.
23. Fewou SN, Ramakrishnan H, Bussow H, Gieselmann V, Eckhardt M. 2007. Down-regulation of polysialic acid is required for efficient myelin formation. J Biol Chem 282:16700-16711. (Pubitemid 47100371)
24. Frost EE, Buttery PC, Milner R, ffrench-Constant C. 1999. Integrins mediate a neuronal survival signal for oligodendrocytes. Curr Biol 9: 1251-1254.
25. Gard AL, Maughon RH, Schachner M. 1996. In vitro oligodendroglio-trophic properties of cell adhesion molecules in the immunoglobulin superfamily: myelin-associated glycoprotein and N-CAM. J Neurosci Res 46:415-426.
26. Hardy RJ, Friedrich VL Jr. 1996. Progressive remodeling of the oligodendrocyte process arbor during myelinogenesis. Dev Neurosci 18:243-254.
27. Jakovcevski I, Mo Z, Zecevic N. 2007. Down-regulation of the axonal polysialic acid-neural cell adhesion molecule expression coincides with the onset of myelination in the human fetal forebrain. Neuroscience 149:328-337. (Pubitemid 47576541)
28. Johnson CP, Fujimoto I, Perrin-Tricaud C, Rutishauser U, Leckband D. 2004. Mechanism of homophilic adhesion by the neural cell adhesion molecule: use of multiple domains and flexibility. Proc Natl Acad Sci U S A 101:6963-6968. (Pubitemid 38596426)
29. Kiselyov VV, Skladchikova G, Hinsby AM, Jensen PH, Kulahin N, Soroka V, Pedersen N, Tsetlin V, Poulsen FM, Berezin V, Bock E. 2003. Structural basis for a direct interaction between FGFR1 and NCAM and evidence for a regulatory role of ATP. Structure 11:691-701. (Pubitemid 37281184)
30. Kiselyov VV, Soroka V, Berezin V, Bock E. 2005. Structural biology of NCAM homophilic binding and activation of FGFR. J Neurochem 94:1169-1179. (Pubitemid 41232573)
31. Klementiev B, Novikova T, Novitskaya V, Walmod PS, Dmytriyeva O, Pakkenberg B, Berezin V, Bock E. 2007. A neural cell adhesion molecule- derived peptide reduces neuropathological signs and cognitive impairment induced by Abeta(25-35). Neuroscience 149:931-942. (Pubitemid 46227730)
32. Klementiev B, Novikova T, Korshunova I, Berezin V, Bock E. 2008. The NCAM-derived P2 peptide facilitates recovery of cognitive and motor function and ameliorates neuropathology following traumatic brain injury. Eur J Neurosci 27:2885-2896. (Pubitemid 351832212)
33. Meiri KF, Saffell JL, Walsh FS, Doherty P. 1998. Neurite outgrowth stimulated by neural cell adhesion molecules requires growth-associated protein-43 (GAP-43) function and is associated with GAP-43 phosphorylation in growth cones. J Neurosci 18:10429-10437. (Pubitemid 29016562)
34. Neiiendam JL, Kohler LB, Christensen C, Li S, Pedersen MV, Ditlevsen DK, Kornum MK, Kiselyov VV, Berezin V, Bock E. 2004. An NCAM-derived FGF-receptor agonist, the FGL-peptide, induces neurite outgrowth and neuronal survival in primary rat neurons. J Neurochem 91:920-935. (Pubitemid 39507369)
35. Niethammer P, Delling M, Sytnyk V, Dityatev A, Fukami K, Schachner M. 2002. Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 157:521-532. (Pubitemid 34839814)
36. Payne HR, Lemmon V. 1993. Glial cells of the O-2A lineage bind preferentially to N-cadherin and develop distinct morphologies. Dev Biol 159:595-607. (Pubitemid 23334083)
37. Ranheim TS, Edelman GM, Cunningham BA. 1996. Homophilic adhesion mediated by the neural cell adhesion molecule involves multiple immunoglobulin domains. Proc Natl Acad Sci U S A 93:4071-4075.
38. Rougon G, Agostini-Bazin H, Hirn M, Goridis C. 1982. Tissue- and developmental stage-specific forms of a neural cell surface antigen linked to differences in glycosylation of a common polypeptide. EMBO J 1: 1239-1244.
39. Saffell JL, Ashton SV, Walsh FS, Doherty P. 1992. The changing role of NCAM as a neurite outgrowth-promoting molecule during development. Biochem Soc Trans 20:410-412.
40. Saffell JL, Williams EJ, Mason IJ, Walsh FS, Doherty P. 1997. Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs. Neuron 18:231-242. (Pubitemid 27111106)
41. Secher T, Novitskaia V, Berezin V, Bock E, Glenthoj B, Klementiev B. 2006. A neural cell adhesion molecule-derived fibroblast growth factor receptor agonist, the FGL-peptide, promotes early postnatal sensorimotor development and enhances social memory retention. Neuroscience 141:1289-1299. (Pubitemid 44128675)
42. Sherman DL, Brophy PJ. 2005. Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6:683-690.
43. Skibo GG, Lushnikova IV, Voronin KY, Dmitrieva O, Novikova T, Klementiev B, Vaudano E, Berezin VA, Bock E. 2005. A synthetic NCAM-derived peptide, FGL, protects hippocampal neurons from ischemic insult both in vitro and in vivo. Eur J Neurosci 22:1589-1596. (Pubitemid 41482947)
44. Soroka V, Kiryushko D, Novitskaya V, Ronn LC, Poulsen FM, Holm A, Bock E, Berezin V. 2002. Induction of neuronal differentiation by a peptide corresponding to the homophilic binding site of the second Ig module of the neural cell adhesion molecule. J Biol Chem 277:24676-24683. (Pubitemid 34951998)
45. Taveggia C, Thaker P, Petrylak A, Caporaso GL, Toews A, Falls DL, Einheber S, Salzer JL. 2008. Type III neuregulin-1 promotes oligodendrocyte myelination. Glia 56:284-293.
46. Trapp BD, Nishiyama A, Cheng D, Macklin W. 1997. Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J Cell Biol 137:459-468. (Pubitemid 27181297)
47. Trotter J, Bitter-Suermann D, Schachner M. 1989. Differentiation- regulated loss of the polysialylated embryonic form and expression of the different polypeptides of the neural cell adhesion molecule by cultured oligodendrocytes and myelin. J Neurosci Res 22:369-383. (Pubitemid 19145619)
48. Williams EJ, Furness J, Walsh FS, Doherty P. 1994a. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin. Neuron 13:583-594. (Pubitemid 24300164)
49. Williams EJ, Walsh FS, Doherty P. 1994b. The production of arachidonic acid can account for calcium channel activation in the second messenger pathway underlying neurite outgrowth stimulated by NCAM, N-cadherin, and L1. J Neurochem 62:1231-1234. (Pubitemid 24064541)
50. Wu HY, Dawson MR, Reynolds R, Hardy RJ. 2001. Expression of QKI proteins and MAP1B identifies actively myelinating oligodendrocytes in adult rat brain. Mol Cell Neurosci 17:292-302. (Pubitemid 32176486)
51. Zhou YX, Flint NC, Murtie JC, Le TQ, Armstrong RC. 2006. Retroviral lineage analysis of fibroblast growth factor receptor signaling in FGF2 inhibition of oligodendrocyte progenitor differentiation. Glia 54: 578-590.