Regeneration of brainstem-spinal axons after lesion and immunological disruption of myelin in adult rat

Experimental Neurology

Volumn 154, Issue 1, 1998, Pages 12-22

  Dyer, Jason K ^a   Bourque, Jason A ^a   Steeves, John D ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Galactocerebroside; Red nucleus; Rubrospinal; Serum complement; Spinal cord

Indexed keywords

MYELIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; DEMYELINATION; FEMALE; MACROPHAGE; MICROGLIA; NERVE FIBER REGENERATION; NERVE LESION; NONHUMAN; PRIORITY JOURNAL; RAT; RED NUCLEUS; SPINAL CORD; ULTRASTRUCTURE;

EID: 0032213454     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1998.6905     Document Type: Article

References (59)

1. Armstrong D. Supraspinal contributions to the initiation and control of locomotion in the cat. Prog. Neurobiol. 26:1986;273-361.
2. Bandtlow C. E., Schwab M. E. Purification and biochemical characterization of rat and bovine CNS myelin associated neurite growth inhibitors NI-35 and NI-250. Soc. Neurosci. Abstr. 17:1991;1495.
3. Bregman B. S., Kunkel-Bagden E., Reier P. J., Ning Dai H., McAtee M., Gao D. Recovery of function after spinal cord injury: Mechanisms underlying transplant-mediated recovery of function differ after spinal cord injury in newborn and adult rats. Exp. Neurol. 123:1993;3-16.
4. Bregman B. S., Kunkel-Bagden E., Schnell L., Dal H. N., Gao D., Schwab M. E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature. 378:1995;498-501.
5. Brown L. T. Rubrospinal projections in the rat. J. Comp. Neurol. 154:1974;169-188.
6. Caroni P., Schwab M. E. Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J. Cell Biol. 106:1988a;1281-1288.
7. Caroni P., Schwab M. E. Antibody against myelin-associated inhibitor of neurite outgrowth neutralizes non-permissive substrate properties of CNS white matter. Neuron. 1:1988b;85-96.
8. Cheng H., Cao Y., Olsen L. Spinal cord repair in adult paraplegic rats: Partial restoration of hindlimb function. Science. 273:1996;510-513.
9. Crutcher K. A. Tissue sections from the mature rat brain and spinal cord as substrates for neurite outgrowth in vitro: Extensive outgrowth on gray matter but little growth on white matter. Exp. Neurol. 104:1989;39-54.
10. David S., Aguayo A. J. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science. 214:1981;931-933.
11. Davis G. R., McClellan A. D. Extent and time course of restoration of descending brainstem projections in spinal-cord transected lamprey. J. Comp. Neurol. 344:1994;65-82.
12. Dorfman S. H., Fry J. M., Silberberg D. H. Antiserum induced demyelination inhibitionin vitro. Brain Res. 177:1979;105-114.
13. Doucette R. Olfactory ensheathing cells can be induced to express a myelinating phenotype. Cell Biology and Pathology of Myelin. 1997;Plenum Press, New York. p. 335-345.
14. Dubios-Dalcq M., Niedieck B., Buyse M. Action of anti-cerebroside sera on myelinated tissue cultures. Pathol. Eur. 5:1970;331-347.
15. Dyer C. A., Benjamins J. A. Glycolipids and transmembrane signaling: Antibodies to galactocerebroside cause an influx of calcium in oligodendrocytes. J. Cell Biol. 111:1990;625-633.
16. Dyer C. A., Matthieu J. M. Antibodies to myelin/oligodendrocyte-specific protein and myelin/oligodendrocyte glycoprotein signal distinct changes in the organization of cultured oligodendroglial membrane sheets. J. Neurochem. 62:1994;777-787.
17. Fry J. M., Weissbarth S., Lehrer G. M., Burnstein M. B. Cerebroside antibody inhibits sulfatide synthesis and myelination and demyelination in cord tissue cultures. Science. 183:1974;540-542.
18. Hasan S. J., Keirstead H. S., Muir G. D., Steeves J. D. Axonal regeneration contributes to repair of injured brainstem-spinal neurons in embryonic chick. J. Neurosci. 13:1993;492-507.
19. Hasan S. J., Nelson B. H., Valenzuela J. I., Keirstead H. S., Schull S. E., Ethell D. W., Steeves J. D. Functional repair of transected spinal cord in embryonic chick. Restor. Neurol. Neurosci. 2:1991;137-154.
20. Heimer L., Zaborszky L. Neuroanatomical tract-tracing methods 2: Recent Progress. 1989;Plenum, New York.
21. Houle J. D. Demonstration of the potential for chronically injured neurons to regenerate axons into intraspinal peripheral nerve grafts. Exp. Neurol. 113:1991;1-9.
22. Hruby S., Alroul E. C. Jr., Seil F. J. Synthetic galactocerebroside evoke myelination-inhibiting antibodies. Science. 195:1977;173-175.
23. Huisman A. M., Kuypers H. G. J. M., Verburgh C. A. Quantitative differences in collateralization of the descending spinal pathways from red nucleus and other brainstem sell groups in rat as demonstrated with the multiple fluorescent retrograde tracer technique. Brain Res. 209:1981;217-286.
24. Iwashita Y., Kawaguchi S., Murata M. Restoration of function by replacement of spinal cord segments in the rat. Nature. 367:1994;167-170.
25. Keirstead H. S., Levine J. M., Blakemore W. F. The response of the oligodendrocyte progenitor population (as defined by NG2 labeling) to demyelination of the adult spinal cord. Glia. 22:1998;161-170.
26. Keirstead H. S., Dyer J. K., Sholomenko G. N., McGraw J., Delaney K. R., Steeves J. D. Axonal regeneration and physiological activity following transection and immunological disruption of myelin within the hatchling chick spinal cord. J. Neurosci. 15:1995;6963-6974.
27. Keirstead H. S., Hasan S. J., Muir G. D., Steeves J. D. Suppression of the onset of myelination extends the permissive period for the functional repair of embryonic spinal cord. Proc. Natl. Acad. Sci. USA. 89:1992;11664-11668.
28. Keirstead H. S., Pataky D. M., McGraw J., Steeves J. D. In vivo. Brain. Res. Bull. 44:1997;727-734.
29. Li Y., Raisman G. Long axon growth from embryonic neurons transplanted into myelinated tracts of the adult spinal cord. Brain Res. 629:1993;115-127.
30. Li Y., Field P. M., Raisman G. Repair of the adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science. 277:1997;2000-2002.
31. Mayer M. M. Mechanism of cytolysis by complement. Proc. Natl. Acad. Sci. (USA). 69:1972;2954-2958.
32. McKerracher L., David S., Jackson D. L., Kottis V., Dunn R. J., Braun P. E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite outgrowth. Neuron. 13:1994;805-811.
33. Morgan B. P. Complement mediated attack on nucleated cells: Resistance, recovery and non-lethal effects. Biochem. J. 264:1989;1-14.
34. Muir G. D., Steeves J. D. Sensorimotor stimulation to improve locomotor recovery after spinal cord injury. Trends Neurosci. 20:1997;72-77.
35. Mukhopadhyay G., Doherty P., Walsh F. S., Crocker P. R., Filbin M. T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron. 13:1994;757-767.
36. Ranscht B., Clapshaw P. A., Price J., Noble M., Seifert W. Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc. Natl. Acad. Sci. (USA). 79:1982;2709-2713.
37. Richardson P. M., Issa V. M., Aguayo A. J. Regeneration of long spinal axons in the rat. J. Neurocytol. 13:1984;165-182.
38. Richardson P. M., McGuinness U. M., Aguayo A. J. Axons from CNS neurons regenerate into PNS grafts. Nature. 284:1980;264-265.
39. Sahibzada N., Yamasaki D., Rhoades R. W. The spinal and commissural projections from the superior colliculus in then rat and hamster arise from distinct neuronal populations. Brain Res. 415:1987;242-256.
40. Saunders N. R., Balkwill P., Knott G., Habgood M. D., Mollgard K., Treherne J. M., Nicholls J. G. Growth of axons through a lesion in the intact CNS fetal rat maintained in long-term culture. Proc. R. Soc. Lond. B. Biol. 250:1992;171-180.
41. Savio T., Schwab M. E. Rat CNS white matter, but not gray matter, is non-permissive for neuronal cell adhesion and fiber outgrowth. J. Neurosci. 9:1989;1126-1133.
42. Schnell L., Schwab M. E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature. 343:1990;269-272.
43. Schnell L., Schneider R., Kolbeck R., Barde Y-A., Schwab M. E. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature. 367:1994;170-173.
44. Schwab M. E., Bartoldi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76:1996;319-370.
45. Schwab M. E., Caroni P. Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite outgrowth and fibroblast spreading in vitro. J. Neurosci. 8:1988;2381-2393.
46. Schwegler G., Schwab M. E., Kapfhammer J. P. Increased collateral sprouting of primary afferents in the myelin-free spinal cord. J. Neurosci. 15:1995;2756-2767.
47. Sergott R. C., Brown M. J., Silberberg D. H., Lisak R. P. Antigalactocerebroside serum demyelinates optic nerve in vivo. J. Neurol. Sci. 64:1984;297-303.
48. Shamboul K. M. Lumbrosacral predominance of vestibulospinal fiber projection in the rat. J. Comp. Neurol. 192:1980;519-530.
49. Shieh J. Y., Leong S. K., Wong W. C. Origin of the rubrospinal tract in neonatal, developing, and mature rats. J. Comp. Neurol. 214:1983;79-86.
50. Sholomenko G. N., Steeves J. D. Effects of selective spinal cord lesions on hind limb locomotion in birds. Exp. Neurol. 95:1987;403-418.
51. Siegal J. D., Kliot M., Smith G. M., Silver J. A comparison of the regeneration potential of dorsal root fibers into gray or white matter of the adult rat spinal cord. Exp. Neurol. 109:1990;90-97.
52. Steeves J. D., Keirstead H. S., Ethell D. W., Hasan S. J., Muir G. D., Pataky D. M., McBride C. B., Petrausch B., Zwimpfer T. J. Permissive and restrictive periods for brainstem-spinal regeneration in the chick. Prog. Brain Res. 103:1994;243-262.
53. Treherne J. M., Woodward S. K. A., Varga Z. M., Ritchie J. M., Nicholls J. G. Restoration of conduction and growth of axons through injured spinal cord of neonatal opossum in culture. Proc. Natl. Acad. Sci. USA. 89:1992;431-434.
54. Varga Z. M., Bandtlow C. E., Erulkar S. D., Schwab M. E., Nicholls J. G. The critical period of repair of CNS neonatal opossum (Monodelphis domestica) in culture: Correlation with development of glial cells, myelin and growth inhibitory molecules. Eur. J. Neurosci. 7:1995;2119-2129.
55. Waldron H. A., Gwyn D. G. Descending nerve tracts of the spinal cord of the rat. I. Fibers from the midbrain. J. Comp. Neurol. 137:1969;143-154.
56. Xu X. M., Guénard V., Kleitman N., Aebischer P., Bunge M. B. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 138:1995;261-276.
57. Yakovleff A., Cabelguen J-M., Orsal D., Gimenez y Robotta M., Rajaofetra N., Drian M-J., Bussel B., Privat A. Fictive activities in adult chronic spinal rats transplanted with embryonic brainstem neurons. Exp. Brain Res. 106:1995;69-78.
58. Ye J. H., Houle J. D. Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143:1997;70-81.
59. Zemlan F. P., Kow L-M., Morrell J. I., Pfaff D. W. Descending tracts of the lateral columns of the rat spinal cord: A study using the horseradish peroxidase and silver impregnation techniques. J. Anat. 128:1979;489-512.