European Journal of Neuroscience, Vol. 10, pp. 680–688, 1998 © European Neuroscience Association
Focal ischaemia of the rat brain elicits an unusual
inflammatory response: early appearance of CD8+
macrophages/microglia
Sebastian Jander, Michael Schroeter, Donatella D’Urso, Clemens Gillen, Otto W. Witte and Guido Stoll
Department of Neurology and Center for Biological and Medical Research, Heinrich-Heine-University, PO Box 10 10 07,
D-40001 Du
¨
sseldorf, Germany
Keywords: CD4, experimental autoimmune encephalomyelitis, Wallerian degeneration.
Abstract
Cerebral ischaemia leads to profound glial activation and leukocyte infiltration into the infarct area. In this study,
we provide evidence for a dual macrophage response in focal ischaemic lesions of the rat brain. We show that a
considerable proportion of macrophages in the ischaemic lesions express the CD8αβ heterodimer to date only
described on CD8+ T cells. As known from other lesion paradigms, CD4+ macrophages were also present.
Interestingly, CD8- and CD4-expressing macrophages formed two non-overlapping subpopulations. CD8+
macrophages reached their maximum during the first week with pronounced downregulation thereafter whereas
CD4+ cells persisted at high levels into the second week. In contrast to cerebral ischaemia, macrophages in the
spleen and in Wallerian degeneration after optic nerve axotomy expressed CD4, but not CD8. In experimental
autoimmune encephalomyelitis, CD8 was mainly associated with T cells and very weakly detectable on some
ramified cells resembling activated microglia. In conclusion, we show that cerebral ischaemia triggers an unusual
inflammatory response characterized by the appearance of CD8+/CD4– macrophages that might exert specific
functions in the pathogenesis of ischaemic brain damage.
Introduction
Both resident microglia and infiltrating blood-derived macrophages
contribute to the population of activated macrophages that appear in
response to different kinds of central nervous system (CNS) injury
(Perry & Gordon, 1988; Streit et al., 1988; Perry et al., 1993; Schroeter
et al., 1997). Activated CNS macrophages can exert cytotoxic effector
functions (Banati et al., 1993; Giulian et al., 1993). In neurological
disorders like stroke and spinal cord injury, these cells may therefore
exacerbate the tissue damage induced by the primary ischaemic or
traumatic insult (Giulian & Robertson, 1990; Lees, 1993; Dusart &
Schwab, 1994; Gehrmann et al., 1995). On the other hand, activated
macrophages secrete growth promoting substances and remove inhibit-
ory tissue debris (Lindholm et al., 1987; Schwab & Caroni, 1988;
David et al., 1990). Thereby, they are equally important in repair and
regeneration processes after CNS injury.
Irrespective of the underlying disease mechanism, activated CNS
macrophages uniformly upregulate immunomolecules—most promin-
ently major histocompatibility complex (MHC) class II and CD4
antigens—on their surface (Matsumoto et al., 1986; Perry & Gordon,
1987; Stoll et al., 1989; Streit et al., 1989; Matsushima et al., 1994).
To date, no phenotypic markers that could differentiate functionally
specialized macrophage subpopulations in the injured CNS have been
described. We have previously shown that the macrophage response
to focal cerebral ischaemia in the rat is accompanied by the appearance
Correspondence: Sebastian Jander, as above.
Received 20 March 1997, revised 18 August 1997, accepted 6 October 1997
of substantial numbers of CD8+ cells (Schroeter et al., 1994; Jander
et al., 1995). These cells do not express markers for T cells or natural
killer (NK) cells, the only two established CD8+ cell populations in
the rat (Lawetzky et al., 1990; Torres-Nagel et al., 1992). In the
present study, we used double labelling immunofluorescence in
combination with confocal microscopy and mRNA analysis by reverse
transcriptase–polymerase chain reaction (RT–PCR) to study the pre-
cise cellular localization and time course of CD8 expression in
ischaemic lesions induced by either middle cerebral artery occlusion
(MCAO) or photothrombosis of cortical microvessels (Watson et al.,
1985). We provide evidence that CD8 after ischaemia is expressed
on a hitherto unrecognized subpopulation of activated CNS macro-
phages that may play a specific functional role in the pathogenesis
of ischaemic brain damage.
Materials and methods
Animals
Focal cerebral infarcts were induced in adult male Wistar and female
Lewis rats by permanent MCAO or photothrombosis of cortical
microvessels as described in detail elsewhere (Schroeter et al., 1994;
Jander et al., 1995). Animals were killed 24 h later and on days 3, 6, 10
and 14 after ischaemia. Experimental autoimmune encephalomyelitis