Ectopic expression of polysialylated neural cell adhesion molecule in adult Macaque Schwann cells promotes their migration and remyelination potential in the central nervous system

Brain

Volumn 133, Issue 2, 2010, Pages 406-420

  Bachelin, C ^a,b,c   Zujovic, V ^a,b,c   Buchet, D ^a,b,c   Mallet, J ^a,b,c   Baron Van Evercooren, A ^a,b,c  

^a INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c CNRS   (France)

Author keywords

CNS; Migration; Remyelination; Schwann cells; STX

Indexed keywords

GREEN FLUORESCENT PROTEIN; NERVE CELL ADHESION MOLECULE; SIALYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGENICITY; ARTICLE; ASTROCYTE; CELL MIGRATION; CELL THERAPY; CELL TRANSPLANTATION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEMYELINATION; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MACACA; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMYELINIZATION; SCHWANN CELL; SPINAL CORD;

EID: 77249123338     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awp256     Document Type: Article

References (51)

1. Angata K, Fukuda M. Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie 2003; 85: 195-206.
2. Avellana-Adalid V, Bachelin C, Lachapelle F, Escriou C, Ratzkin B, Baron-Van Evercooren A. In vitro and in vivo behaviour of NDF-expanded monkey Schwann cells. Eur J Neurosci 1998; 10: 291-300.
3. Bachelin C, Lachapelle F, Girard C, Moissonnier P, Serguera-Lagache C, Mallet J, et al. Efficient myelin repair in the macaque spinal cord by autologous grafts of Schwann cells. Brain 2005; 128: 540-549
4. Baron-Van Evercooren A, Avellana-Adalid V, Ben Younes-Chennoufi A, Gansmuller A, Nait-Oumesmar B, Vignais L. Cell-cell interactions during the migration of myelin-forming cells transplanted in the demyelinated spinal cord. Glia 1996; 16: 147-164
5. Baron-Van Evercooren A, Avellana-Adalid V, Lachapelle F, Liblau R. Schwann cell transplantation and myelin repair of the CNS. Mult Scler 1997; 3: 157-161
6. Baron-Van Evercooren A, Gansmuller A, Duhamel E, Pascal F, Gumpel M. Repair of a myelin lesion by Schwann cells transplanted in the adult mouse spinal cord. J Neuroimmunol 1992; 40: 235-242
7. Black JA, Waxman SG, Smith KJ. Remyelination of dorsal column axons by endogenous Schwann cells restores the normal pattern of Nav1.6 and Kv1.2at nodes of Ranvier. Brain 2006; 129: 1319-1329
8. Blakemore WF. Remyelination of CNS axons by Schwann cells transplanted from the sciatic nerve. Nature 1977; 266: 68-69
9. Blakemore WF, Franklin RJ. Transplantation options for therapeutic central nervous system remyelination. Cell Transplant 2000; 9: 289-294
10. Charneau P, Alizon M, Clavel F. A second origin of DNA plus-strand synthesis is required for optimal human immunodeficiency virus replication. J Virol 1992; 66: 2814-2820
11. Coman I, Aigrot MS, Seilhean D, Reynolds R, Girault JA, Zalc B, et al. Nodal, paranodal and juxtaparanodal axonal proteins during demyelination and remyelination in multiple sclerosis. Brain 2006; 129: 3186-3195
12. Craner MJ, Lo AC, Black JA, Waxman SG. Abnormal sodium channel distribution in optic nerve axons in a model of inflammatory demyelination. Brain 2003; 126: 1552-1561
13. Decker L, Avellana-Adalid V, Nait-Oumesmar B, Durbec P, Baron-Van Evercooren A. Oligodendrocyte precursor migration and differentiation: combined effects of PSA residues, growth factors, and substrates. Mol Cell Neurosci 2000; 16: 422-439
14. Duncan ID, Aguayo AJ, Bunge RP, Wood PM. Transplantation of rat Schwann cells grown in tissue culture into the mouse spinal cord. J Neurol Sci 1981; 49: 241-252
15. Durbec P, Cremer H. Revisiting the function of PSA-NCAM in the nervous system. Mol Neurobiol 2001; 24: 53-64.
16. Fairless R, Frame MC, Barnett SC. N-cadherin differentially determines Schwann cell and olfactory ensheathing cell adhesion and migration responses upon contact with astrocytes. Mol Cell Neurosci 2005; 28: 253-263
17. Fouad K, Schnell L, Bunge MB, Schwab ME, Liebscher T, Pearse DD. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J Neurosci 2005; 25: 1169-1178
18. Franklin RJ. Remyelination of the demyelinated CNS: the case for and against transplantation of central, peripheral and olfactory glia. Brain Res Bull 2002; 57: 827-832
19. Franklin RJ, Blakemore WF. Requirements for Schwann cell migration within CNS environments: a viewpoint. Int J Dev Neurosci 1993; 11: 641-649
20. Girard C, Bemelmans AP, Dufour N, Mallet J, Bachelin C, Nait-Oumesmar B, et al. Grafts of brain-derived neurotrophic factor and neurotrophin 3-transduced primate Schwann cells lead to functional recovery of the demyelinated mouse spinal cord. J Neurosci 2005; 25: 7924-7933
21. Glaser T, Brose C, Franceschini I, Hamann K, Smorodchenko A, Zipp F, et al. Neural cell adhesion molecule polysialylation enhances the sensitivity of embryonic stem cell-derived neural precursors to migration guidance cues. Stem Cells 2007; 25: 3016-3025
22. Gout O, Gansmuller A, Baumann N, Gumpel M. Remyelination by transplanted oligodendrocytes of a demyelinated lesion in the spinal cord of the adult shiverer mouse. Neurosci Lett 1988; 87: 195-199
23. Hinks GL, Franklin RJ. Delayed changes in growth factor gene expression during slow remyelination in the CNS of aged rats. Mol Cell Neurosci 2000; 16: 542-556
24. Honmou O, Felts PA, Waxman SG, Kocsis JD. Restoration of normal conduction properties in demyelinated spinal cord axons in the adult rat by transplantation of exogenous Schwann cells. J Neurosci 1996; 16: 3199-3208
25. Imaizumi T, Lankford KL, Kocsis JD. Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res 2000; 854: 70-78
26. Jeffery ND, Blakemore WF. Remyelination of mouse spinal cord axons demyelinated by local injection of lysolecithin. J Neurocytol 1995; 24: 775-781
27. Jessen KR, Mirsky R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 2005; 6: 671-682
28. Johnson CP, Fujimoto I, Rutishauser U, Leckband DE. Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem 2005; 280: 137-145
29. Kohama I, Lankford KL, Preiningerova J, White FA, Vollmer TL, Kocsis JD. Transplantation of cryopreserved adult human Schwann cells enhances axonal conduction in demyelinated spinal cord. J Neurosci 2001; 21: 944-950
30. Lakatos A, Barnett SC, Franklin RJ. Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Exp Neurol 2003; 184: 237-246
31. Lasiene J, Shupe L, Perlmutter S, Horner P. No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. J Neurosci 2008; 28: 3887-3896
32. Lavdas AA, Franceschini I, Dubois-Dalcq M, Matsas R. Schwann cells genetically engineered to express PSA show enhanced migratory potential without impairment of their myelinating ability in vitro. Glia 2006; 53: 868-878
33. Levi AD, Bunge RP, Lofgren JA, Meima L, Hefti F, Nikolics K, et al. The influence of heregulins on human Schwann cell proliferation. J Neurosci 1995; 15: 1329-1340
34. McCarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 1980; 85: 890-902.
35. McTigue DM, Horner PJ, Stokes BT, Gage FH. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 1998; 18: 5354-5365
36. Meintanis S, Thomaidou D, Jessen KR, Mirsky R, Matsas R. The neuron-glia signal beta-neuregulin promotes Schwann cell motility via the MAPK pathway. Glia 2001; 34: 39-51.
37. Oumesmar BN, Vignais L, Duhamel-Clerin E, Avellana-Adalid V, Rougon G, Baron-Van Evercooren A. Expression of the highly polysia-lylated neural cell adhesion molecule during postnatal myelination and following chemically induced demyelination of the adult mouse spinal cord. Eur J Neurosci 1995; 7: 480-491
38. Papastefanaki F, Chen J, Lavdas AA, Thomaidou D, Schachner M, Matsas R. Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain 2007; 130: 2159-2174
39. Pearse DD, Marcillo AE, Oudega M, Lynch MP, Wood PM, Bunge MB. Transplantation of Schwann cells and olfactory ensheathing glia after spinal cord injury: does pretreatment with methylprednisolone and interleukin-10 enhance recovery? J Neurotrauma 2004; 21: 1223-1239
40. Ranscht B, Clapshaw PA, Price J, Noble M, Seifert W. Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc Natl Acad Sci USA 1982; 79: 2709-2713
41. Rutishauser U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 2008; 9: 26-35.
42. Rutkowski JL, Kirk CJ, Lerner MA, Tennekoon GI. Purification and expansion of human Schwann cells in vitro. Nat Med 1995; 1: 80-83
43. Santos-Silva A, Fairless R, Frame MC, Montague P, Smith GM, Toft A, et al. FGF/heparin differentially regulates Schwann cell and olfactory ensheathing cell interactions with astrocytes: a role in astrocytosis. J Neurosci 2007; 27: 7154-7167
44. Sasaki M, Black JA, Lankford KL, Tokuno HA, Waxman SG, Kocsis JD. Molecular reconstruction of nodes of Ranvier after remyelination by transplanted olfactory ensheathing cells in the demyelinated spinal cord. J Neurosci 2006; 26: 1803-1812
45. Sommer I, Schachner M. Monoclonal antibodies (O1 to O4) to oligo-dendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 1981; 83: 311-327
46. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 2002; 22: 6670-6681
47. Vitry S, Bertrand JY, Cumano A, Dubois-Dalcq M. Primordial hematopoietic stem cells generate microglia but not myelin-forming cells in a neural environment. J Neurosci 2003; 23: 10724-10731
48. Wilby MJ, Muir EM, Fok-Seang J, Gour BJ, Blaschuk OW, Fawcett JW. N-Cadherin inhibits Schwann cell migration on astrocytes. Mol Cell Neurosci 1999; 14: 66-84.
49. Yoshimura K, Negishi T, Kaneko A, Sakamoto Y, Kitamura K, Hosokawa T, et al. Monoclonal antibodies specific to the integral membrane protein P0 of bovine peripheral nerve myelin. Neurosci Res 1996; 25: 41-49
50. Zennou V, Serguera C, Sarkis C, Colin P, Perret E, Mallet J, et al. The HIV-1 DNA flap stimulates HIV vector-mediated cell transduction in the brain. Nat Biotechnol 2001; 19: 446-450
51. Zujovic V, Bachelin C, Baron-Van Evercooren A. Remyelination of the central nervous system: a valuable contribution from the periphery. Neuroscientist 2007; 13: 383-391