Microglial changes accompanying the promotion of retinal ganglion cell axonal regeneration into peripheral nerve grafts

Journal of Neurocytology

Volumn 31, Issue 1, 2002, Pages 57-71

  Raibon, E ^a   Sauve Y ^b   Carter, D A ^c   Gaillard, F ^a  

^a UNIVERSITÉ DE POITIERS   (France)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ZYMOSAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CELL SURVIVAL; CONTROLLED STUDY; DOSE RESPONSE; FEMALE; GLIA CELL; IMMUNOREACTIVITY; MACROPHAGE ACTIVATION; MICROGLIA; NERVE DEGENERATION; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NERVE GRAFT; NONHUMAN; PERIPHERAL NERVE; PHAGOCYTOSIS; PRIORITY JOURNAL; RETINA GANGLION CELL;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD147; ANTIGENS, NEOPLASM; ANTIGENS, SURFACE; AVIAN PROTEINS; AXONS; BLOOD PROTEINS; CELL COUNT; CRICETINAE; FEMALE; MEMBRANE GLYCOPROTEINS; MESOCRICETUS; MICROGLIA; NERVE REGENERATION; PERIPHERAL NERVES; RATS; RATS, INBRED BN; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS; TRANSPLANTS;

ANIMALIA; CRICETINAE;

EID: 0344407029     PISSN: 03004864     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1022527800181     Document Type: Article

References (56)

1. AURIAULT, C., JOSEPH, M., TARTAR, A., BOUT, D., TONNEL, A. B. & CAPRON, A. (1985) Regulatory role of a tripeptide (TKP) from the second constant domain of immunoglobulin G-I. Inhibition of rat and human macrophage activities. International Journal of Immunopharmacology 7, 73-79.
2. AURIAULT, C., JOSEPH, M., TARTAR, A. & CAPRON, A. (1983) Characterization and synthesis of a macrophage inhibitory peptide from the second constant domain of human immunoglobulin G. FEBS Letters 153, 11-15.
3. AVELLINO, A. M., HART, D., DAILEY, A. T., MCKINNON, M., ELLEGALA, D. & KLIOT, M. (1995) Differential macrophage responses in the peripheral and central nervous system during Wallerian degeneration of axons. Experimental Neurology 136, 183-198.
4. AVILES-TRIGUEROS, M., SAUVÉ, Y., LUND, R. D. & VIDAL-SANZ, M. (2000) Selective innervation of retinorecipient brainstem nuclei by retinal ganglion cell axons regenerating through peripheral nerve grafts in adult rats. Journal of Neuroscience 20, 361-374.
5. BALASINGAM, V. & YONG, V. W. (1996) Attenuation of astroglial reactivity by interleukin-10. Journal of Neuroscience 16, 2945-2955.
6. BATCHELOR, P. E., LIBERATORE, G. T., WONG, J. Y. F., PORRITT, M. J., FRERICHS, F., DONNAN, G. A. & HOWELLS, D. W. (1999) Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell-line derived neurotrophic factor. Journal of Neuroscience 19, 1708-1716.
7. BERKELAAR, M., CLARKE, D., WANG, Y. C., BRAY, G. M. & AGUAYO, A. J. (1994) Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. Journal of Neuroscience 14, 4368-4374.
8. BOHATSCHEK, M., KLOSS, C. U. A., KALLA, R. & RAIVICH, G. (2001) In vitro model of microglial deramification: Ramified microglia transform into ameboid phagocytes following addition of brain cell membranes to microglia-astrocyte cocultures. Journal of Neuroscience Research 64, 508-522.
9. CARTER, D. A., BRAY, G. M. & AGUAYO, A. J. (1989) Regenerated retinal ganglion cell axons can form well-differentiated synapses in the superior colliculus of adult hamsters. Journal of Neuroscience 9, 4042-4050.
10. CARTER, D. A. & JHAVERI, S. (1997) Retino-geniculate axons regenerating in adult hamsters are able to form morphologically distinct terminals. Experimental Neurology 146, 315-322.
11. CHIANELLA, S., SEMPREVIVO, M., PENG, Z.-C., ZACCHEO, D., BENTIVOGLIO, M. & GRASSII-ZUCCONI, G. (1999) Microglia activation in a model of sleep disorder: An immunohistochemical study in the rat brain during Trypanosoma brucei infection. Brain Research 832, 54-62.
12. CHO, K. S., CHAN, P. M., SO, K. F., YIP, H. K. & CHUNG, S. K. (1999) Ciliary neurotrophic factor promotes the regrowth capacity but not the survival of intraorbitally axotomized retinal ganglion cells in adult hamsters. Neuroscience 94, 623-628.
13. CHO, E. Y. & SO, K. F. (1987) Rate of regrowth of damaged retinal ganglion cell axons regenerating in a peripheral nerve graft in adult hamsters. Brain Research 419, 369-374.
14. DAVIS, E. J., FOSTER, T. D. & THOMAS, W. E. (1994) Cellular forms and functions of brain microglia. Brain Research Bulletin 34, 73-78.
15. DEZAWA, M., KAWANA, K., NEGISHI, H. & ADACHI-USAMI, E. (1999) Glial cells in degenerating and regenerating optic nerve of the adult rat. Brain Research Bulletin 48, 573-579.
16. FISCHER, D., PAVLIDIS, M. & THANOS, S. (2000) Cataractogenic lens injury prevents traumatic ganglion cell death and promotes axonal regeneration both in vivo and in culture. Investigative Ophthalmology and Visual Science 41, 3943-3954.
17. GARCIA-VALENZUELA, E. & SHARMA, S. C. (1999) Laminar restriction of retinal macrophagic response to optic nerve axotomy in the rat. Journal of Neurobiology 40, 55-66.
18. GRAEBER, M. B., LOPEZ-REDONDO, F., IKOMA, E., ISHIKAWA, M., IMAI, Y., NAKAJIMA, K., KREUTZBERG, G. W. & KOHSAKA, S. (1998) The microglia/macrophage response in the neonatal rat facial nucleus following axotomy. Brain Research 813, 241-253.
19. GRAEBER, M. B., TETZLAFF, W., STREIT, W. J. & KREUTZBERG, G. W. (1988) Microglial cells but not astrocytes undergo mitosis following rat facial nerve axotomy. Neuroscience Letters 85, 317-321.
20. HIRSCHBERG, D. L. & SCHWARTZ, M. (1995) Macrophage recruitment to acutely injured central nervous system is inhibited by a resident factor: A basis for an immune brain barrier. Journal of Neuroimmunology 61, 89-96.
21. HUGHES, A. (1979) A schematic eye for the rat. Vision Research 19, 569-588.
22. JONES, L. L., KREUTZBERG, G. W. & RAIVICH, G. (1998) Transforming growth factor β's 1, 2, and 3 inhibit proliferation of ramified microglia on an astrocyte monolayer. Brain Research 795, 301-306.
23. KLOSS, C. U. A., KREUZTZBERG, G. W. & RAIVICH, G. (1997) Proliferation of ramified microglia on an astrocyte monolayer: Characterization of stimulatory and inhibitory cytokines. Journal of Neuroscience Research 49, 248-254.
24. KREUTZBERG, G. W. (1996) Microglia: A sensor for pathological events in the CNS. Trends in Neuroscience 19, 312-318.
25. LAWSON, L. J., PERRY, V. H. & GORDON, S. (1992) Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48, 405-415.
26. LAZAROV-SPIEGLER, O., SOLOMON, A. S. & SCHWARTZ, M. (1998) Peripheral nerve-stimulated macrophages simulate a peripheral nerve-like regenerative response in rat transected optic nerve. Glia 24, 329-337.
27. LAZAROV-SPIEGLER, O., SOLOMON, A. S. & SCHWARTZ, M. (1999) Link between optic nerve regrowth failure and macrophage stimulation in mammals. Vision Research 39, 169-175.
28. LEON, S., YIN, Y., NGUYEN, J., IRWIN, N. & BENOWITZ, L. I. (2000) Lens injury stimulates axon regeneration in the mature rat optic nerve. Journal of Neuroscience 20, 4615-4626.
29. LING, E. A. & WONG, W. C. (1993) The origin and nature of ramified and amoeboid microglia: A historical review and current concepts. Glia 7, 9-18.
30. MANSOUR-ROBAEY, S., CLARKE, D. B., WANG, Y. C., BRAY, G. M. & AGUAYO, A. J. (1994) Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proceedings of the National Academy of Sciences USA 91, 1632-1636.
31. PERRY, V. H., BROWN, M. C. & GORDON, S. (1987) The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. Journal of Experimental Medicine 165, 1218-1223.
32. PERRY, V. H. & GORDON, S. (1988) Macrophages and microglia in the nervous system. Trends in Neuroscience 11, 273-277.
33. RAIVICH, G., BOHATSCHECK, M., KLOSS, C. U. A., WERNER, A., JONES, L. L. & KREUTZBERG, G. W. (1999) Neuroglial activation repertoire in the injured brain: Graded response, molecular mechanisms, and cues to physiological function. Brain Research Reviews 30, 77-105.
34. RAO, K. & LUND, R. D. (1993) Optic nerve degeneration induces the expression of MHC antigens in the rat visual system. Journal of Comparative Neurology 336, 613-627.
35. REICHERT, F. & ROTSHENKER, S. (1996) Deficient activation of microglia during optic nerve degeneration. Journal of Neuroimmunology 70, 153-161.
36. ROGOVE, A. D. & TSIRKA, S. E. (1998) Neurotoxic responses by microglia elicited by excitotoxic injury in the mouse hippocampus. Current Biology 8, 19-25.
37. ROQUE, R. S., IMPERIAL, C. J. & CALDWELL, R. B. (1996) Microglial cells invade the outer retina as photoreceptors degenerate in Royal College of Surgeons rats. Investigative Ophthalmology and Visual Sciences 37, 196-203.
38. SALVADOR-SILVA, M., VIDAL-SANZ, M. & VILLEGAS-PEREZ, M. P. (2000) Microglial cells in the retina of Carassius auratus: Effects of optic nerve crush. Journal of Comparative Neurology 417, 431-447.
39. SCHNITZER, J. & SCHERER, J. (1990) Microglial cell responses in the rabbit retina following transection of the optic nerve. Journal of Comparative Neurology 302, 779-791.
40. SO, K. F. & YIP, H. K. (2001) The use of peripheral nerve transplants to enhance axonal regeneration in CNS neurons. In Axonal Regeneration in the Central Nervous System (edited by INGOGLIA, N. A. & MURRAY, M.) pp. 505-528. New York: Marcel Dekker.
41. SOLTYS, Z., ZIAJA, M., PAWLINSKI, R., SETKOWICZ, Z. & JANECKO, K. (2001) Morphology of reactive microglia in the injured cerebral cortex. Fractal analysis and complementary quantitative methods. Journal of Neuroscience Research 63, 90-97.
42. STENCE, N., WAITE, M. & DAILEY, M. E. (2001) Dynamics of microglial activation: A confocal time-lapse analysis in hippocampal slices. Gila 19, 256-266.
43. STICHEL, C. C. & MÜLLER, H. W. (1998) Experimental strategies to promote axonal regeneration after traumatic central nervous system injury. Progress in Neurobiology 56, 119-148.
44. STREIT, W. J., GRAEBER, M. B. & KREUTZBERG, G. W. (1988) Functional plasticity of microglia. A review. Glia 1, 301-307.
45. STREIT, W. J., GRAEBER, M. B. & KREUTZBERG, G. W. (1989) Peripheral nerve lesion produces increased levels of major histocompatibility complex antigens in the central nervous system. Journal of Neuroimmunology 21, 117-123.
46. TERUBAYASHI, H., MURABE, Y., FUJISAWA, H., ITOI, M. & IBATA, Y. (1984) Enzymohistochemical identification of microglial cells in the rat retina: Light and electron microscopy studies. Experimental Eye Research 39, 595-603.
47. THANOS, S. & MEY, J. (1995) Type-specific stabilization and target-dependent survival of regenerating ganglion cells in the retina of adult rats. Journal of Neuroscience 15, 1057-1079.
48. THANOS, S., MEY, J. & WILD, M. (1993) Treatment of the adult retina with microglia-suppressing factors retards axotomy-induced neuronal degradation and enhances axonal regeneration in vivo and in vitro. Journal of Neuroscience 13, 455-466.
49. THANOS, S., MOORE, S. & HONG, Y. M. (1996) Retinal microglia. Progress in Retina and Eye Research 15, 331-361.
50. THANOS, S., NASKAR, R. & HEIDUSCHKA, P. (1997) Regenerating ganglion cell axons in the adult rat establish retinofugal topography and restore visual function. Experimental Brain Research 114, 483-491.
51. VIDAL-SANZ, M., BRAY, G. M., VILLEGAS-PEREZ, M. P., THANOS, S. & AGUAYO, A. (1987) Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. Journal of Neuroscience 7, 2894-2909.
52. VILLEGAS-PEREZ, M. P., VIDAL-SANZ, M., BRAY, G. M. & AGUAYO, A. (1988) Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. Journal of Neuroscience 8, 265-280.
53. WHITELEY, S. J. O., SAUVÉ, Y., AVILES-TRIGUEROS, M., VIDAL-SANZ, M. & LUND, R. D. (1998) Extent and duration of recovered pupillary light reflex following retinal ganglion cell axon regeneration through peripheral nerve grafts directed to the pretectum in adult rats. Experimental Neurology 154, 560-572.
54. WILMS, P. & BÄHR, M. (1995) Reactive changes in the adult rat superior colliculus after deafferentation. Restorative Neurology and Neuroscience 9, 21-34.
55. WIZENMANN, A. & BÄHR, M. (1997) Growth characteristics of ganglion cell axons in the developing and regenerating retino-tectal projection of the rat. Cell and Tissue Research 290, 395-403.
56. ZHANG, J., WU, G.-S., ISHIMOTO, S.-I., PARARAJASEGARAM, G. & RAO, N. A. (1997) Expression of major histocompatibility complex molecules in rodent retina. Investigative Ophthalmology and Visual Science 38, 1848-1857.