Transplantation of oligodendrocyte progenitor cells into the rat retina: Extensive myelination of retinal ganglion cell axons

GLIA

Volumn 18, Issue 3, 1996, Pages 200-210

  Laeng, Pascal ^a   Molthagen, Martin ^a   Gui Xia Yu, Ester ^a   Bartsch, Udo ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Lamina cribrosa; Migration; Myelin; Oligodendrocyte; Tenascin C

Indexed keywords

ANIMAL; ARTICLE; CELL TRANSPLANTATION; CYTOLOGY; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MYELIN SHEATH; NERVE FIBER; OLIGODENDROGLIA; PHYSIOLOGY; RAT; RETINA; RETINA GANGLION CELL; RNA PROBE; SPRAGUE DAWLEY RAT; STEM CELL; STEM CELL TRANSPLANTATION; TRANSPLANTATION; ULTRASTRUCTURE;

ANIMALS; AXONS; CELL TRANSPLANTATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROSCOPY, ELECTRON; MYELIN SHEATH; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RETINA; RETINAL GANGLION CELLS; RNA PROBES; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 0030293006     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1136(199611)18:3<200::AID-GLIA4>3.0.CO;2-2     Document Type: Article

References (59)

1. Barnett, S.C., Franklin, R.J.M., and Blakemore, W.F. (1993) In vitro and in vivo analysis of a rat bipotential O-2A progenitor cell line containing the temperature-sensitive mutant gene of the SV40 large T antigen. Eur. J. Neurosci., 5:1247-1260.
2. Bartsch, S., Bartsch, U., Dörries, U., Faissner, A., Weller, A., Ekblom, P., and Schachner, M. (1992) Expression of tenascin in the developing and adult cerebellar cortex. J. Neurosci., 12:736-749.
3. Bartsch, U. (1996) The extracellular matrix molecule tenascin-C: Expression in vivo and functional characterization in vitro. Prog. Neurobiol., 49:145-168.
4. Bartsch, U., Kirchhoff, F., and Schachner, M. (1989) Immunohistological localization of the adhesion molecules L1, N-CAM, and MAG in the developing and adult optic nerve of mice. J. Comp. Neurol., 284:451-462.
5. Bartsch, U., Bartsch, S., Dörries, U., and Schachner, M. (1992) Immunohistological localization of tenascin in the developing and lesioned adult mouse optic nerve. Eur. J. Neurosci., 4:338-352.
6. Bartsch, U., Faissner, A., Trotter, J., Dörries, U., Bartsch, S., Mohajeri, H., and Schachner, M. (1994) Tenascin demarcates the boundary between the myelinated and nonmyelinated part of retinal ganglion cell axons in the developing and adult mouse. J. Neurosci., 14:4756-4768.
7. Bartsch, U., Montag, D., Bartsch, S., and Schachner, M. (1995) Multiply myelinated axons in the optic nerve of mice deficient for the myelin-associated glycoprotein. Glia, 14:115-122.
8. Baulac, M., Lachapelle, F., Gout, O., Berger, B., Baumann, N., and Gumpel, M. (1987) Transplantation of oligodendrocytes in the newborn mouse brain: Extension of myelination by transplanted cells. Anatomical study. Brain Res., 420:39-47.
9. Berliner, M.L. (1931) Cytologic studies on the retina. I. Normal coexistence of oligodendroglia and myelinated nerve fibers. Arch. Ophthalmol., 6:740-751.
10. Berry, M., Hall, S., Follows, R., and Wyse, J.P.H. (1989) Defective myelination in the optic nerve of the Browman-Wyse (BW) mutant rat. J. Neurocytol., 18:141-159.
11. Besnard, F., Perraud, F., Sensenbrenner, M., and Labourdette, G. (1989) Effects of acidic and basic fibroblast growth factors on proliferation and maturation of cultured rat oligodendrocytes. Int. J. Dev. Neurosci., 7:401-409.
12. Blakemore, W.F. and Franklin, R.J.M. (1991) Transplantation of glial cells into the CNS. TINS, 14:323-327.
13. Bögler, O., Wren, D., Barnett, S.C., Land, H., and Noble, M. (1990) Cooperation between two growth factors promotes extended selfrenewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc. Natl. Acad. Sci. USA, 87:6368-6372.
14. Büssow, H. (1978) Schwann cell myelin ensheathing C.N.S. axons in the nerve fibre layer of the cat retina. J. Neurocytol., 7:207-214.
15. Crang, A.J. and Blakemore, W.F. (1991) Remyelination of demyelinated rat axons by transplanted mouse oligodendrocytes. Glia, 4:305-313.
16. Dörries, U., Bartsch, U., Nolte, C., Roth, J., and Schachner, M. (1993) Adaption of a non-radioactive in situ hybridization method to electron microscopy: Detection of tenascin mRNAs in mouse cerebellum with digoxigenin-labelled probes and gold-labelled antibodies. Histochemistry, 99:251-262.
17. Eisenbarth, G.S., Walsh, F.S., and Nirenberg, M. (1979) Monoclonal antibody to a plasma membrane antigen of neurons. Proc. Natl. Acad. Sci. USA, 76:4913-4917.
18. Espinosa de los Monteros, A., Zhang, M.S., and de Vellis, J. (1993) O-2A progenitor cells transplanted into the neonatal rat brain develop into oligodendrocytes but not astrocytes. Proc. Natl. Acad. Sci. USA, 90:50-54.
19. ffrench-Constant, C., Miller, R.H., Burne, J.F., and Raff, M.C. (1988) Evidence that migratory oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve. J. Neurocytol., 17:13-25.
20. Flage, T. (1977) Permeability properties of the tissues in the optic nerve head region in the rabbit and the monkey. Acta Ophthalmol., 55:652-664.
21. Forrester, F. and Peters, A. (1967) Nerve fibers in optic nerve of rat. Nature, 214:245-247.
22. Franklin, R.J.M. and Blakemore, W.F. (1995) Glial-cell transplantation and plasticity in the O-2A lineage - implications for CNS repair. TINS, 18:151-156.
23. Franklin, R.J.M., Bayley, S.A., Milner, R., ffrench-Constant, C., and Blakemore, W.F. (1995) Differentiation of the O-2A progenitor cell line CG-4 into oligodendrocytes and astrocytes following transplantation into glia-deficient areas of CNS white matter. Glia, 13:39-44.
24. Fulton, B.P., Burne, J.F., and Raff, M.C. (1992) Visualization of O-2A progenitor cells in developing and adult rat optic nerve by quisqualate-stimulated cobalt uptake. J. Neurosci., 12:4816-4833.
25. Gansmuller, A., Clerin, E., Krüger, F., Gumpel., M., and Lachapelle, F. (1991) Tracing transplanted oligodendrocytes during migration and maturation in the shiverer mouse brain. Glia, 4:580-590.
26. +GalC) under different mitogenic control. Neuron, 5:615-625.
27. Groves, A.K., Barnett, S.C., Franklin, R.J.M., Crang, A.J., Mayer, M., Blakemore, W.F., and Noble, M. (1993) Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells. Nature, 362:453-455.
28. Gumpel., M., Baumann, N., Raoul., M., and Jacque, C. (1983) Survival and differentiation of oligodendrocytes from neural tissue transplanted into newborn mouse brain. Neurosci. Lett., 37:307-311.
29. Hildebrand, C., Remahl., S., and Waxman, S.G. (1985) Axo-glial relations in the retina-optic nerve junction of the adult rat: Electronmicroscopic observations. J. Neurocytol., 14:597-617.
30. Huang, P.P., Alliquant, B., Carmel., P.W., and Friedman, E.D. (1991) Myelination of the rat retina by transplantation of oligodendrocytes into 4-day-old hosts. Exp. Neural., 113:291-300.
31. Jacque, C., Quinonero, J., Collins, P.V., Villarroya, H., and Suard, I. (1992) Comparative migration and development of astroglial and oligodendroglial cell populations from a brain xenograft. J. Neurosci., 12:3098-3106.
32. Jung, H.J., Raine, C.S., and Suzuki, K. (1978) Schwann cells and peripheral nervous system myelin in the rat retina. Acta Neuropathol., 44:245-247.
33. Jung, M., Krämer, E., Grzenkowski, M., Tang, K., Blakemore, W., Aguzzi, A., Khazaie, K., Chlichlia, K., von Blankenfeld, G., Kettenmann, H., and Trotter, J. (1995) Lines of murine oligodendroglial precursor cells immortalized by an activated neu tyrosine kinase show distinct degrees of interaction with axons in vitro and in vivo. Eur. J. Neurosci., 7:1245-1265.
34. Kiernan, B.W. and ffrench-Constant, C. (1993) Oligodendrocyte precursor (O-2A progenitor cell) migration; a model system for the study of cell migration in the developing central nervous system. Development (Suppl.), 219-225.
35. Lachapelle, F., Lapie, P., Nussbaum, J.L., and Gumpel., M. (1990) Immunohistochemical studies on cross-transplantations between jimpy, shiverer, and normal newborn mice. J. Neurosci. Res., 27:324-331.
36. Lachapelle, F., Duhamel-Clerin, E., Gansmüller, A., Baron-Van Evercooren, A., Villarroya, H., and Gumpel., M. (1994) Transplanted transgenically marked oligodendrocytes survive, migrate and myelinate in the normal mouse brain as they do in the shiverer mouse brain. Eur. J. Neurosci., 6:814-824.
37. Laeng, P., Décimo, D., Pettmann, B., Janet, T., and Labourdette, G. (1994) Retinoic acid regulates the development of oligodendrocyte precursor cells in vitro. J. Neurosci. Res., 39:613-633.
38. Laeng, P., Molthagen, M., Gui-Xia Yu, E., and Bartsch, U. (1996) Transplanted oligodendrocyte progenitors extensively myelinate rat retinal ganglion cell axons. J. Neurochem., 66:S92.
39. McKinnon, R.D., Smith, C., Behar, T., Smith, T., and Dubois-Dalq, M. (1993) Distinct effects of bFGF and PDGF on oligodendrocyte progenitor cells. Glia, 7:245-254.
40. Mitrovic, N. and Schachner, M. (1995) Detection of tenascin-C in the nervous system of the tenascin-C mutant mouse. J. Neurosci. Res., 42:710-717.
41. Mudhar, H.S., Pollock, R.A., Wang, C., Stiles, C.D., and Richardson, W.D. (1993) PDGF and its receptors in the developing rodent retina and optic nerve. Development, 118:539-552.
42. Nave, K.-A., Lai, C., Bloom, F.E., and Milner, R.J. (1986) Jimpy mutant mouse: A 74-base deletion in the mRNA for myelin proteolipid protein and evidence for a primary defect in RNA splicing. Proc. Natl. Acad. Sci. USA, 83:264-9268.
43. Perry, V.H. and Hayes, L. (1985) Lesion-induced myelin formation in the retina. J. Neurocytol., 14:297-307.
44. Perry, V.H. and Lund, R.D. (1990) Evidence that the lamina cribrosa prevents intraretinal myelination of retinal ganglion cell axons. J. Neurocytol., 19:265-272.
45. Poltorak, M., Sadoul., R., Keilhauer, G., Landa, C., Fahrig, T., and Schachner, M. (1987) The myelin-associated glycoprotein (MAG), a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuron-oligodendrocyte and oligodendrocyte-oligodendrocyte interaction. J. Cell Biol., 105:1893-1899.
46. Raff, M.C., Miller, R.H., and Noble, M. (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature, 303:390-396.
47. Saga, Y., Yagi, T., Ikawa, Y., Sakakura, T., and Aizawa, S. (1992) Mice develop normally without tenascin. Genes Dev., 6:1821-1831.
48. Schachner, M., Kim, S.K., and Zehnle, R. (1981) Developmental expression in central and peripheral nervous system of oligodendrocyte cell surface antigens (O antigens) recognized by monoclonal antibodies. Dev. Biol., 83:328-338.
49. Schnitzer, J. (1985) Distribution and immunoreactivity of glia in the retina of the rabbit. J. Comp. Neurol., 240:128-142.
50. Skoff, R.P., Knapp, P.E., and Bartlett, W.P. (1986) Astrocytic diversity in the optic nerve: A cytoarchitectural study. In: Astrocytes: Vol. I. S. Federoff and A. Vernadakis, eds. Academic Press, New York, pp. 269-291.
51. Small., R.K., Riddle, P., and Noble, M. (1987) Evidence for migration of oligodendrocyte-type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature, 328:155-157.
52. Sommer, I. and Schachner, M. (1981) Monoclonal antibodies (O1 to 04) to oligodendrocyte cell surfaces: An immunocytological study in the central nervous system. Dev. Biol., 83:311-327.
53. Sugimoto, T., Fukuda, Y., and Wakakuwa, K. (1984) Quantitative analysis of a cross-sectional area of the optic nerve: A comparison between albino and pigmented rats. Exp. Brain Res., 54:266-274.
54. Trotter, J., Crang, A.J., Schachner, M., and Blakemore, W.F. (1993) Lines of glial precursor cells immortalized with a temperature-sensitive oncogene give rise to astrocytes and oligodendrocytes following transplantation into demyelinated lesions in the central nervous system. Glia, 9:25-40.
55. Tso, M.O.M., Shih, C.-Y., and McLean, I.W. (1975) Is there a bloodbrain barrier at the optic nerve head? Arch. Ophthalmol., 93: 815-825.
56. Utzschneider, D.A., Archer, D.R., Kocsis, J.D., Waxman, S.G., and Duncan, I.D. (1994) Transplantation of glial cells enhances action potential conduction of amyelinated spinal cord axons in the myelindeficient rat. Proc. Natl. Acad. Sci. USA, 91:53-57.
57. Warrington, A.E., Barbarese, E., and Pfeiffer, S.E. (1993) Differential myelinogenic capacity of specific developmental stages of the oligodendrocyte lineage upon transplantation into hypomyelinating hosts. J. Neurosci. Res., 34:1-13.
58. Wyse, J.P.H. (1980) Schwann cell myelination in the nerve fibre layer of the BW rat retina. J. Neurocytol., 9:107-117.
59. Wyse, J.P.H. and Spira, A.W. (1981) Ultrastructural evidence of a peripheral nervous system pattern of myelination in the avascular retina of the guinea pig. Acta Neuropathol., 54:203-210.