Elsevier

Journal of Chemical Neuroanatomy

Volume 6, Issue 4, July–August 1993, Pages 267-275
Journal of Chemical Neuroanatomy

Induction of microglial immunomolecules by anterogradely degenerating mossy fibres in the rat hippocampal formation

https://doi.org/10.1016/0891-0618(93)90048-9Get rights and content

Abstract

Degeneration of myelinated axonal connections is generally held to provide a strong stimulus for microglial expression of major histocompatibility complex (MHC) class II antigen. The present study demonstrates that strong microglial reactions also are induced by axonal and terminal degeneration of the unmyelinated hippocampal mossy fibres. After destruction of denate granule cells by focal injections of colchicine (or transection of the mossy fibres) in adult rats, immunocytochemical analysis of the mossy fibre terminal fields in the dentate hilus and regio inferior of hippocampus proper (CA3) revealed profound changes in microglial cells with increased expression of the complement receptor type 3 and induction of MHC class I antigen, leukocyte common antigen, lymphocyte function-associated antigen-1 and MHC class II antigen. The microglial reaction, first detectable 4 days after the lesion, became maximal during the third postlesional week, and had almost vanished 6 weeks after the lesion.

From recent studies we know that anterograde degeneration of myelinated Schaffer-collaterals from CA3 to regio superior of hippocampus proper and myelinated entorhinal perforant path fibres to fascia dentata is accompanied by microglial expression of MHC class I antigen, but not class II. Together with the present findings, this demonstrates that myelin debris is neither necessary nor sufficient to induce expression of microglial MHC class II antigen within the hippocampus.

References (55)

  • H. Konno et al.

    Wallerian degeneration induces Ia-antigen expression in the rat brain

    J. Neuroimmunol.

    (1989)
  • P.A. Lapchak et al.

    Immunoautoradiographic localization of interleukin 2-like immunoreactivity and interleukin 2 receptors (Tac antigen-like immunoreactivity) in the rat brain

    Neuroscience

    (1991)
  • D.A. Matthews et al.

    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.

    (1976)
  • J.V. Nadler et al.

    Loss and reacquisition of hippocampal synapses after selective destruction of CA3–CA4 afferents with kainic acid

    Brain Res.

    (1980)
  • M. Nieto-Sampedro et al.

    Growth factors and growth factor receptors in the hippocampus

  • E.G. Pedersen et al.

    MHC expression in blood-brain barrier deficient areas of the normal rat brain

    J. Neuroimmunol. Suppl

    (1991)
  • K. Rao et al.

    Degeneration of optic axons induces the expression of major histocompatibility antigens

    Brain Res.

    (1989)
  • Th.J. Walsh et al.

    Colchicine induced granule cell loss in rat hippocampus: Selective behavioural and histological alterations

    Brain Res.

    (1986)
  • M.R. Wells et al.

    Changes in plasma cytokines associated with peripheral nerve injury

    J. Neuroimmunol.

    (1992)
  • K.T. Yee et al.

    Differential expression of class I and class II major histocompatibility complex antigen in early postnatal rats

    Brain Res.

    (1990)
  • D.G. Amaral et al.

    Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions

    J. Comp. Neurol.

    (1981)
  • C.R. Bandtlow et al.

    Regional and cellular codistribution of interleukin 1β and nerve growth factor mRNA in the adult rat brain: Possible relationship to the regulation of nerve growth factor synthesis

    Nature (Lond.)

    (1990)
  • D.I. Beller et al.

    Regulation of macrophage populations. II. synthesis and expression of Ia antigens by peritoneal exudate macrophages is a transient event

    J. Immunol.

    (1981)
  • T.W. Blackstad et al.

    Special axodendritic synapses in the hippocampal cortex: Electron and light microscopic studies on the layer of mossy fibers

    J. Comp. Neurol.

    (1961)
  • G.G. Borisy et al.

    The mechanism of action of colchicine

    Binding of colchicine-3H to cellular protein

    J. Cell Biol.

    (1967)
  • A.L. Carbonell et al.

    Ultrastructural study of the neuroglial and macrophagic reaction in Wallerian degeneration of the adult rat optic nerve

    Histol. Histopath.

    (1991)
  • B.R. Finsen et al.

    Microglial MHC antigen expression after ischemic and kainic acid lesions of the adult rat hippocampus

    Glia

    (1993)
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