Microglial reactivity correlates to the density and the myelination of the anterogradely degenerating axons and terminals following perforant path denervation of the mouse fascia dentata

Neuroscience

Volumn 93, Issue 2, 1999, Pages 507-518

  Jensen, M B ^a,b   Hegelund, I V ^a   Poulsen, F R ^a   Owens, T ^b   Zimmer, J ^a   Finsen, B ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Anterograde axonal degeneration; Glial cells; Hippocampus; Mouse; Myelin

Indexed keywords

CD11B ANTIGEN; MYELIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DENERVATION; DENSITOMETRY; DENTATE GYRUS; HIPPOCAMPUS; IMMUNOREACTIVITY; MICROGLIA; MORPHOLOGY; MOUSE; MYELINATION; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL;

ANIMALS; AXONS; COLORING AGENTS; DENSITOMETRY; DENTATE GYRUS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICROGLIA; MYELIN BASIC PROTEINS; MYELIN SHEATH; NERVE DEGENERATION; OLIGODENDROGLIA; PERFORANT PATHWAY; PRESYNAPTIC TERMINALS; SILVER STAINING; TOLONIUM CHLORIDE;

EID: 0032777771     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00139-6     Document Type: Article

References (46)

1. Amaral D. G. and Witter M. P. (1995) The hippocampal formation. In The Rat Nervous System, (ed. Paxinos G.), 2nd edn., pp. 443-493. Academic, San Diego.
2. Andersson P.B., Perry V.H., Gordon S. The kinetics and morphological characteristics of the macrophage-microglial response to kainic acid-induced neuronal degeneration. Neuroscience. 42:1991;201-214.
3. Berger T., Frotscher M. Distribution and morphological characteristics of oligodendrocytes in the rat hippocampus in situ and in vitro: an immunohistochemical study with the monoclonal RiP antibody. J. Neurocytol. 23:1994;61-74.
4. Blakemore W. F., Crang A. J. and Evans R. J. (1983) The effect of chemical injury on oliogodendrocytes. In Viruses and Demyelinating Diseases (eds Mims C. A., Cuzner M. L. and Kelly R. I.), pp. 167-190. Academic, London.
5. Bregman B.S., Kunkel-Bagden E., Schnell L., Dai H.N., Gao D., Schwab M.E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature. 378:1995;498-501.
6. Caroni P., Schwab M.E. Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron. 1:1988;85-96.
7. Cotman C.W., Nieto-Sampedro M. Brain function, synapse renewal and plasticity. A. Rev. Psychol. 33:1982;371-401.
8. Daniel P.M., Strich S.J. Histological observations on the Wallerian degeneration in the spinal cord of the baboon Papio papio. Acta neuropath. 12:1969;314-328.
9. del Rio-Hortega P., Penfield W. The reaction of neuroglia and microglia to brain wounds. Bull. Johns Hopkins Hosp. 41:1919;278-303.
10. Deller T., Frotscher M., Nitsch R. Morphological evidence for the sprouting of inhibitory commissural fibers in response to the lesion of the excitatory entorhinal input to the rat dentate gyrus. J. Neurosci. 15:1995;6868-6878.
11. Deller T., Nitsch R., Frotscher M. Layer-specific sprouting of commissural fibers to the rat fascia dentata after unilateral entorhinal cortex lesion: a Phaseolus vulgaris leucoagglutinin tracing study. Neuroscience. 71:1996;651-660.
12. D'Souza S.D., Bonetti B., Balasingam V., Cashman N.R., Barker P.A., Troutt A.B., Raine C.S., Antel J.P. Multiple sclerosis: Fas signalling in oligodendrocyte cell death. J. exp. Med. 184:1996;2361-2370.
13. Fagan A.M., Gage F.H. Cholinergic sprouting in the hippocampus, a proposed role for IL-1. Expl Neurol. 110:1990;105-120.
14. Finsen B.R., Jørgensen M.B., Diemer N.H., Zimmer J. Microglial MHC antigen expression after ischemic and kainic acid lesions of the adult rat hippocampus. Glia. 7:1993;41-49.
15. Finsen B.R., Tønder N., Xavier G., Sørensen J.C., Zimmer J. Induction of microglial immunomolecules by anterogradely degenerating mossy fibers in the rat hippocampal formation. J. chem. Neuroanat. 6:1993;267-275.
16. Franson P., Ronnevi L.-O. Myelin breakdown and elimination in the posterior funiculus of the adult cat after dorsal rhizotomy: a light and electron microscopic qualitative and quantitative study. J. comp. Neurol. 223:1984;138-151.
17. Friedman B., Hockfield S., Black J.A., Woodruff K.A., Waxman S.G. In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody RIP. Glia. 2:1989;380-390.
18. Frotscher M., Heimrich B., Deller T. Sprouting in the hippocampus is layer specific. Trends Neurosci. 20:1997;218-223.
19. Frotscher M., Leranth C. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J. comp. Neurol. 239:1985;237-246.
20. Gall C., Rose G., Lynch G. Proliferative and migratory activity of glial cells in the partially deafferented hippocampus. J. comp. Neurol. 183:1979;539-550.
21. Hildebrand C. Electron-microscopic identification of Gomori-positive rings in normal spinal cord white matter. Acta neuropath. 56:1982;29-34.
22. Hildebrand C., Remahl S., Persson H., Bjartmar C. Myelinated nerve fibres in the CNS. Prog. Neurobiol. 40:1993;319-384.
23. Hjorth-Simonsen A. Fink-Heimer silver impregnation of degenerating axons and terminals in mounted cryostat sections of fresh and fixed brains. Stain Tech. 45:1970;199-204.
24. Hjorth-Simonsen A. Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J. comp. Neurol. 146:1972;219-232.
25. Hjorth-Simonsen A., Jeune B. Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. comp. Neurol. 144:1972;215-232.
26. Jensen M.B., Finsen B., Zimmer J. Morphological and immunophenotypic microglial changes in the denervated fascia dentata of adult rats: correlation with blood-brain barrier damage and astroglial reactions. Expl Neurol. 143:1997;103-116.
27. Jensen M.B., González B., Castellano B., Zimmer J. Microglial and astroglial reactions to anterograde axonal degeneration: a histochemical and immunocytochemical study of the adult rat fascia dentata after entorhinal perforant path lesions. Expl Brain Res. 98:1994;245-260.
28. Kalwy S.A., Smith R. Mechanisms of myelin basic protein and proteolipid protein targeting in oligodendrocytes. Molec. Membr. Biol. 11:1994;67-78.
29. Li M., Shibata A., Li C., Braun P.E., McKerracher L., Roder J., Kater S.B., David S. Myelin-associated glycoprotein inhibits neurite/axon growth and causes growth cone collapse. J. Neurosci. Res. 46:1996;404-414.
30. Linington C., Webb M., Woodhams P.L. A novel myelin associated glycoprotein defined by a mouse monoclonal antibody. J. Neuroimmunol. 6:1984;387-396.
31. Ludwin S.K. Phagocytosis in the rat optic nerve following Wallerian degeneration. Acta neuropath. 80:1990;266-273.
32. Ludwin S.K., Bisby M.A. Delayed Wallerian degeneration in the central nervous system of Ola mice: an ultrastructural study. J. neurol. Sci. 109:1992;140-147.
33. Lyon M.F., Ogunklade B.W., Brown M.C., Atherton D.J., Perry V.H. A gene affecting Wallerian nerve degeneration maps distally on mouse chromosomes 4. Proc. natn. Acad. Sci. U.S.A. 90:1993;9717-9720.
34. Matthews D.A., Cotman C., Lynch G. An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration. Brain Res. 115:1976;1-21.
35. 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 growth. Neuron. 13:1994;805-811.
36. McNaughton B.L. Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res. 119:1980;1-19.
37. Ozawa K., Suchanek G., Breitschopf H., Brück W., Budka H., Jellinger K., Lassmann H. Patterns of oligodendroglia pathology in multiple sclerosis. Brain. 117:1994;1311-1322.
38. Perry V.H., Hume D.A., Gordon S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience. 15:1985;313-326.
39. Persson H., Berthold C.H. Cellular relationships of paranodal Marchi-positive bodies studied with monoclonal antibodies against partially degraded CNS myelin fragments. J. Neurocytol. 20:1991;277-289.
40. Prayoonwiwat N., Rodriguez M. The potential for oligodendrocyte proliferation during demyelinating disease. J. Neuropath. exp. Neurol. 52:1993;55-63.
41. Smetanka A.M., Yee K.T., Lund R.D. Differential induction of class I and II MHC antigen expression by degenerating myelinated and unmyelinated axons. Brain Res. 521:1990;343-346.
42. Sternberger N.H., Itoyama Y., Kies M.W., Webster H. DeF. Myelin basic protein demonstrated immunocytochemically in oligodendroglia prior to myelin sheath formation. Proc. natn. Acad. Sci. U.S.A. 75:1978;2521-2524.
43. Steward O. Signals that induce sprouting in the central nervous system: sprouting is delayed in a strain of mouse exhibiting delayed axonal degeneration. Expl Neurol. 118:1992;340-351.
44. West M.J., Østergaard K., Andreassen O.A., Finsen B. Estimation of the number of somatostatin neurons in the striatum: an in situ hybridization study using the optical fractionator method. J. comp. Neurol. 370:1996;11-22.
45. Zimmer J. Extended commissural and ipsilateral projections in postnatally deentorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation. Brain Res. 64:1973;293-311.
46. Zimmer J., Finsen B., Sørensen T., Poulsen P.H. Xenografts of mouse hippocampal tissue. Exchange of laminar and neuropeptide specific nerve connections with the host rat brain. Brain Res. Bull. 20:1988;369-379.