Genetic influences on cellular reactions to brain injury: Activation of microglia in denervated neuropil in mice carrying a mutation (Wld(S)) that causes delayed Wallerian degeneration

Journal of Comparative Neurology

Volumn 380, Issue 1, 1997, Pages 82-94

  Schauwecker, P Elyse ^a   Steward, Oswald ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

CR3 receptor; entorhinal cortex; glia; Mac 1 immunocytochemistry; regeneration

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; DENERVATION; GENE MUTATION; IMMUNOCYTOCHEMISTRY; MALE; MICROGLIA; MOUSE; NERVE DEGENERATION; NERVE ENDING; NERVE FIBER; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; SYNAPSE;

ACID ANHYDRIDE HYDROLASES; ANIMALS; AXONS; DENDRITES; DENERVATION; DENTATE GYRUS; ENTORHINAL CORTEX; HISTOCYTOCHEMISTRY; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; MICROGLIA; POINT MUTATION; TIME FACTORS; WALLERIAN DEGENERATION;

EID: 0030891013     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970331)380:1<82::AID-CNE6>3.0.CO;2-P     Document Type: Article

References (85)

1. Angelov, D.N., A. Gunkel, E. Stennert, and W.F. Neiss (1995) Phagocytic microglia during delayed neuronal loss in the facial nucleus of the rat: Time course of the neuronofugal migration of brain macrophages. Glia 13:113-129.
2. Araujo, D.M., and C.W. Cotman (1992) Beta-amyloid stimulates growth factors that acculumate in senile plaques in Alzheimer's disease. Brain Res. 569:141-145.
3. Banati, R.B., J. Gehrmann, C. Czech, U. Mönning, L.L. Jones, G. König, K. Beyreuther, and G.W. Kreutzberg (1993) Early and rapid de novo-synthesis of Alzheimer βA4-amyloid precursor protein (APP) in activated microglia. Glia 9:199-210.
4. Barnard, J.A., C.C. Bascom, M.M. Lyons, N.J. Sipes, and H.L. Moses (1988) Transforming growth factor β in the control of epidermal proliferation. Am. J. Med. Sci. 296:159-163.
5. Battisti, W.P., J. Wang, K. Bozek, and M. Murray (1995) Macrophages, microglia, and astrocytes are rapidly activated after crush injury of the goldfish optic nerve: A light and electron microscopic analysis. J. Comp. Neurol. 354:306-320.
6. Blackstad, T.W. (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J. Comp. Neurol. 105:417-537.
7. Brown, M.C., E.R. Lunn, and V.H. Perry (1992) Consequences of slow Wallerian degeneration for regenerating motor and sensory axons. J. Neurobiol. 223:521-536.
8. Castellano, B., B. Gonzalez, B.R. Finsen, and J. Zimmer (1990) Histochemical demonstration of purine nucleoside phosphorylase (PNPase) in microglial and astroglial cells of adult rat brain. J. Histochem. Cytochem. 38:1535-1539.
9. Castellano, B., B. Gonzalez, M.B. Jensen, E.B. Pedersen, B.R. Finsen, and J. Zimmer (1991) A double immunostaining technique for simultaneous demonstration of astrocytes and microglia in brain sections and astroglial cell cultures. J. Histochem. and Cytochem. 39:561-568.
10. Chen, S., and M.A. Bisby (1993) Impaired motor axon regeneration in the C57BL/Ola mouse. J. Comp. Neurol. 333:449-454.
11. Cotman, C.W., and G. Lynch (1976) Reactive synaptogenesis in the hippocampus. In S.H. Barondes (ed): Neuronal Recognition. London: Chapman and Hall, pp. 69-104.
12. Cotman, C.W., and J.V. Nadler (1978) Reactive synaptogenesis in the hippocampus. In C.W. Cotman (ed): Neuronal Plasticity. New York: Raven Press, pp. 227-272.
13. Deckwerth, T.L., and E.M. Johnson, Jr. (1994) Neurites can remain viable after destruction of the neuronal soma by programmed cell death (apoptosis). Dev. Biol. 165:64-72.
14. del Rio-Hortega, P. (1932) Microglia. In X.W. Penfield (ed): Cytology and Cellular Pathology of the Nervous System. Vol. 2. New York: P.B. Hoeber, pp. 481-534.
15. Eclancher, F., F. Perraud, J. Faltin, G. Labourdette, and M. Sensenbrenner (1990) Reactive astrogliosis after basic fibroblast growth factor (bFGF) injection in injured neonatal rat brain. Glia 3:502-509.
16. Fagan, A.M., and F.H. Gage (1990) Cholinergic sprouting in the hippocampus: A proposed role for IL-1. Exp. Neurol. 110:105-120.
17. Falcone, D.J., T.A. McCaffrey, A. Haimovitz-Friedman, and M. Garcia (1993) Transforming growth factor-beta 1 stimulates macrophage urokinase expression and release of matrix-bound basic fibroblast growth factor. J. Cell. Phys. 155:595-605.
18. Fearon, D.T., and W.W. Wong (1983) Complement ligand-receptor interactions that mediate biological responses. Ann. Rev. Immunol. 1:243-271.
19. Fink, R.P., and L. Heimer (1967) Two methods for selective silver impregnation of degeneration axons and their synaptic endings in the central nervous system. Brain Res. 4:369-374.
20. Finsen, B.R., T. Sorensen, B. Castellano, E.B. Pedersen, and J. Zimmer (1991) Leucocyte infiltration and glial reactions in xenografts of mouse brain tissue undergoing rejection in the adult rat brain. A light and electronmicroscopical immunocytochemical study. J. Neuroimmunol. 32:159-183.
21. Finsen, B.R., M.B. Jorgensen, N.H. Diemer, and J. Zimmer (1993) Microglial MHC antigen expression after ischemic and kainic acid lesions of the adult rat hippocampus. Glia 7:41-49.
22. S) that causes delayed Wallerian degeneration. J. Comp. Neurol. 317:469-484.
23. Gage, F.H., P. Olejniczak, and D. Armstrong (1988) Astrocytes are important for sprouting in the septohippocampal circuit. Exp. Neurol. 102: 2-13.
24. Gall, C., G. Rose, and G. Lynch (1979) Proliferative and migratory activity of glial cells in the partially deafferented hippocampus. J. Comp. Neurol. 183:539-550.
25. Gehrmann, J., S.W. Schoen, and G.W. Kreutzberg (1991) Lesion of the rat entorhinal cortex leads to a rapid microglial reaction in the dentate gyrus. A light and electron microscopic study. Acta Neuropath. 82:442-455.
26. George, R., and J.W. Griffin (1994) Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: The dorsal radiculotomy model. Exp. Neurol. 125:225-236.
27. Giulian, D., and T.J. Baker (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 6:2163-2178.
28. Giulian, D., and L.B. Lachman (1985) Interleukin-1 stimulation of astroglial proliferation after brain injury. Science 228:497-498.
29. Giulian, D., and C. Robertson (1990) Inhibition of mononuclear phagocytes reduces ischemic injury in the spinal cord. Ann. Neurol. 27:33-42.
30. Giulian, D., and D.G. Young (1986) Brain peptides and glial growth. II. Identification of cells that secrete glia-promoting factors. J. Cell Biol. 102:812-820.
31. Giulian, D., J. Woodward, J.F. Krebs, and L.B. Lachman (1988) Intracerebral injections of interleukin-1 stimulates astrogliosis and neovascularization. J. Neurosci. 8:2485-2490.
32. Giulian, D., J. Li, X. Li, J. George, and P.A. Rutecki (1994) The impact of microglia-derived cytokines upon gliosis in the CNS. Dev. Neurosci. 16:128-136.
33. Glass, J.D., B.L. Schryer, and J.W. Griffin (1994) Calcium-mediated degeneration of the axonal cvtoskeleton in the Ola mouse. J. Neurochem. 62:2472-2475.
34. Gomez-Pinilla, F., J.W.-K. Lee, and C.W. Cotman (1992) Basic FGF in adult rat brain: Cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J. Neurosci. 12:345-355.
35. Graeber, M.B., W.J. Streit, and G.W. Kreutzberg (1988) Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J. Neurosci. Res. 21:18-24.
36. Guthrie, K.M., T. Nguyen, and C.M. Gall (1995) Insulin-like growth factor-1 mRNA is increased in deafferented hippocampus: Spatiotemporal correspondence of a trophic event with axon sprouting. J. Comp. Neurol. 352:147-160.
37. Hatten, M.E., R.K. Liem, M.L. Shelanski, and C.A. Mason (1991) Astroglia in CNS injury. Glia 4:233-243.
38. Hoff, S.F., S.W. Scheff, L.S. Benardo, and C.W. Cotman (1982a) Lesion-induced synaptogenesis in the dentate gyrus of aged rats: II. Demonstration of an impaired degeneration clearing response. J. Comp. Neurol. 205:253-259.
39. Hoff, S.F., S.W. Scheff, L.S. Benardo, and C.W. Cotman (1982b) Lesion-induced synaptogenesis in the dentate gyrus of aged rats. I. Loss and reacquisition of normal synaptic density. J. Comp. Neurol. 204:246-252.
40. Ip, N.Y., S.J. Wiegand, J. Morse, and J.S. Rudge (1993) Injury-induced regulation of ciliary neurtrophic factor mRNA in the adult rat brain. Eur. J. Neurosci. 5:25-33.
41. Jensen, M.B., B. Gonzalez, B. Castellano, and J. Zimmer (1994) Microglial and astroglial reactions to anterograde axonal degeneration: A histochemical and immunocytochemical study of the adult rat fascia dentata after entorhinal perforant path lesions. Exp. Brain Res. 98:245-260.
42. Kreutzberg, G.W. (1996) Microglia - a sensor for pathlogical events in the CNS. Trends Neurosci. 19:312-318.
43. Lawson, L.J., L. Frost, J. Risbridger, S. Fearn, and V.H. Perry (1994) Quantification of the mononuclear phagocyte response to Wallerian degeneration of the optic nerve. J. Neurocytol. 23:729-744.
44. Lee, K., E. Stanford, C.W. Cotman, and G.S. Lynch (1977) Ultrastructural evidence for bouton sprouting in the adult mammalian brain. Exp. Brain Res. 29:475-485.
45. Lindholm, D., R. Heumann, M. Meyer, and H. Thoenen (1987) Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve. Nature 330:658-660.
46. Lindsay, R.M. (1986) Reactive gliosis. In S. Federoff and A. Vernadakis (eds): Astrocytes: Cell Biology and Pathology of Astrocytes, Vol. 3. Orlando, FL: Academic Press, pp. 231-262.
47. Liu, H.M., L.H. Yang, and Y.J. Yang (1995) Schwann cell properties: 3. C-fos expression, bFGF production, phagocytosis and proliferation during Wallerian degeneration. J. Neuropath. Exp. Neurol. 54:487-496.
48. Lunn, E.R., V.H. Perry, M.C. Brown, H. Rosen, and S. Gordon (1989) Absence of Wallerian degeneration does not hinder regeneration in peripheral nerves. Eur. J. Neurosci. 1:27-33.
49. Lynch, G.S., Smith, R.L., and C.W. Cotman (1976) Recovery of function following brain damage: a consideration of some neural mechanisms. In A.A. Buerger and J.S. Tobis (eds): Neurophysiological Aspects of Rehabilitation Medicine. Illinois: Thomas, pp. 280-298.
50. Matthews, D.A., C. Cotman, and G. Lynch (1976a) 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. 115:1-21.
51. Matthews, D.A., C. Cotman, and G. Lynch (1976b) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the rat: II. Reappearance of morphologically normal synaptic contacts. Brain Res. 115:23-41.
52. McLaurin, J., G. Almazan, K. Williams, and J.P. Antel (1995) Immortalization and characterization of rat microglial cells. Neuropath. Appl. Neurobiol. 21:302-311.
53. McWilliams, J.R., and G.S. Lynch (1978) Terminal proliferation and synaptogenesis following partial deafferentation. J. Comp. Neurol. 180:581-616.
54. Mizuno, T., M. Sawada, T. Marunouchi, and A. Suzumura (1994) Production of interleukin-10 by mouse glial cells in culture. Biochem. Biophys. Res. Comm. 205:1907-1915.
55. Morgan, T.E., N.R. Nichols, G.M. Pasinetti, and C.E. Finch (1993) TGF-beta 1 mRNA increases in macrophage/microglial cells of the hippocampus in response to deafferentation and kainic-acid induced neurodegeneration. Exp. Neurol. 120:291-301.
56. Nafstad, P.H. (1967) An electron microscope study on the termination of the perforant path fibres in the hippocampus and the fascia dentata. Zeitschrift Fur Zellforschung Und Mikropskopische Anatomie 76:532-542.
57. Nichols, N.R., N.J. Laping, J.R. Day, and C.E. Finch (1991) Increases in transforming growth factor-beta mRNA in hippocampus during response to entorhinal cortex lesions in intact and adrenalectomized rats. J. Neurosci. Res. 28:134-139.
58. Perry, V.H., Hume, D.A., and S. Gordon (1985) Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neurosci. 15:313-326.
59. Perry, V.H., M.C. Brown, and S. Gordon (1987) The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J. Exp. Med. 165:1218-1223.
60. Perry, V.H., E.R. Lunn, M.C. Brown, S. Cahusac, and S. Gordon (1990a) Evidence that the rate of Wallerian degeneration is controlled by a single autosomal dominant gene. Eur. J. Neurosci. 2:408-413.
61. Perry, V.H., M.C. Brown, E.R. Lunn, P. Tree, and S. Gordon (1990b) Evidence that very slow Wallerian degeneration in C57BL/Ola mice is an intrinsic property of the peripheral nerve. Eur. J. Neurosci. 2:802-808.
62. Perry, V.H., M.C. Brown, and E.R. Lunn (1991) Very slow retrograde and Wallerian degeneration in the CNS of C57BL/Ola mice. Eur. J. Neurosci. 3:102-105.
63. Perry, V.H., P-B. Andersson, and S. Gordon (1993) Macrophages and inflammation in the central nervous system. Trends Neurosci. 16:268-273.
64. Rappolee, D.A., D. Mark, M.J. Banda, and Z. Werb (1988) Wound macrophages express TGF-alpha and other growth factors in vivo: Analysis by mRNA phenotyping. Science 241:708-712.
65. Reier, P.J. (1986) Gliosis following CNS injury: The anatomy of astrocytic scars and their influences on axonal elongation. In S. Federoff and A. Vernadakis (eds): Astrocytes: Cell Biology and Pathology of Astrocytes, Vol. 3. Orlando, FL: Academic Press, pp. 263-324.
66. Riva-Depaty, I., C. Fardeau, J. Mariani, C. Bouchaud, and N. Delhaye-Bouchaud (1994) Contribution of peripheral macrophages and microglia to the cellular reaction after mechanical or neurotoxin-induced lesions of the rat brain. Exp. Neurol. 128:77-87.
67. Sawada, M., A. Suzumura, Y. Itoh, and T. Marunouchi (1993) Production of interleukin-5 by mouse astrocytes and microglia in culture. Neurosci. Lett. 155:175-178.
68. Sawada, M., A. Suzumura, and T. Marunouchi (1995) Induction of functional interleukin-2 receptor in mouse microglia. J. Neurochem. 64:1973-1979.
69. Schelper, R.L., and E.K. Adrian, Jr. (1980) Non-specific esterase activity in reactive cells in injured nervous tissue labeled with 3H-thymidine or 125iododeoxyuridine injected before injury. J. Comp. Neurol. 194:829-844.
70. Schelper, R.L., and E.K. Adrian, Jr. (1986) Monocytes become macrophages; they do not become microglia: A light and electron microscopic autoradiographic study using 125-iododeoxyuridine. J. Neuropath. Exp. Neurol. 45:1-19.
71. Steward, O. (1982) Events within the sprouting neuron and the denervated neuropil during lesion-induced synaptogenesis. In A. Morrison and P. Strick (eds): Changing Concepts of the Nervous System. New York: Academic Press, pp. 33-48.
72. Steward, O. (1986) Lesion-induced synapse growth in the hippocampus: In search of cellular and molecular mechanisms. In R.L. Isaacson and K.H. Pribram (eds): The Hippocampus, Vol. 3. New York: Plenum Press, pp. 65-107.
73. Steward, O. (1989) Reorganization of neuronal connections following trauma: Principles and experimental paradigms. J. Neurotrauma 6:99-152.
74. Steward, O. (1992) Signals that induce sprouting in the central nervous system: Sprouting is delayed in a strain of mouse exhibiting delayed axonal degeneration. Exp. Neurol. 118:340-351.
75. Steward, O., E.R. Torre, L.L. Phillips, and P.A. Trimmer (1990) The process of reinnervation in the dentate gyrus of adult rats: Time course of increases in mRNA for glial fibrillary acidic-protein. J. Neurosci. 10:2373-2384.
76. S) that causes delayed Wallerian degeneration. J. Comp. Neurol. (in press).
77. Stoll, G., B.D. Trapp, and J.W. Griffin (1989) Macrophage function during Wallerian degeneration of rat optic nerve: Clearance of degenerating myelin and la expression. J. Neurosci. 9:2327-2355.
78. Streit, W.J. (1990) An improved staining method for rat microglial cells using the lectin from Griffonia simplicifolia (GSA I-B4). J. Histochem. Cytochem. 38:1683-1686.
79. Streit, W.J. and G.W. Kreutzberg (1988) Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J. Comp. Neurol. 268:248-263.
80. Thanos, S., J. Mey, and M. Wild (1993) Treatment of the adult retina with microglia-suppressing factors retards axotomy-induced neuronal degeneration and enhances axonal regeneration in vivo and in vitro. J. Neurosci. 13:455-466.
81. Thanos, S., J. Kacza, J. Seeger, and J. Mey (1994) Old dyes for new scopes: The phagocytosis-dependent long-term fluorescence labelling of microglial cells in vivo. Trends Neurosci. 17:177-182.
82. Wilson, M.A., and M.E. Molliver (1994) Microglial response to degeneration of serotonergic axon terminals. Glia 11:18-34.
83. Wright, S.D., P.E. Rao, W.C. Van Voorhis, L.S. Craigmyle, K. Iida M.A. Talle, E.F. Westberg, G. Goldstein, and S.C. Silverstein (1983) Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies. Proc. Natl. Acad. Sci. 80:5699-5703.
84. Wyss-Coray, T., L. Feng, E. Masliah, M.D. Ruppe, H.S. Lee, S.M. Toggas, E.M. Rockenstein, and L. Mucke (1995) Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am. J. Path. 147:53-67.
85. Zhang, Z., M. Fujiki, L. Guth, and O. Steward (1996) Genetic influences on cellular reactions to spinal cord injury: A wound healing response present in normal mice is impaired in mice carrying a mutation that causes delayed Wallenan degeneration. J. Comp. Neurol. 371:484-495.