Lymphocytes play the music but the
macrophage calls the tune
Werner Solbach, Heidrun Moll and
Martin Röllinghoff
Macrophages as hosts for microbes
The fate of intracellular parasites
is strongly influenced by their mech-
anis m of attachment to, and pen-
etration of, host cells. Toxoplasma
gondii tachyzoites, for example, can
either actively invade their host and
survive or can be phagocytosed and
arekilled (K.Joiner, New Haven). In
the former case, laminin adsorbed to
the tachyzoite surface binds to the
integrin-ßl receptors on the cell
surface. Entering via this route,
T oxoplasma take up residence in
vacuoles that exdude host mem-
brane glycoproteins. Such vacuoles
fail to fuse with acidifying lysosomes
and endosomes thus protecting the
parasites from lethaI host responses.
However, jf the tachyzoites are
coated with antibody, they are
bound by macrophage Fc receptors
(FcR); the blocks in fusion and acidi-
fication of the vacuoles are overcome
and the microbes are killed by trig-
gering the macrophage's respiratory
burst. The mechanism of this FcR-
mediated reversal of the block in
fusion and acidification is not yet
dear but studies using respiratory-
burst-negative ceIls transfected with
various FcR mutants have shown
that distinct domains of the cyto-
plasmic tail of the FcR direct endo-
cytosis and phagocytosis.
Leishmania adopt a different en-
try and survival strategy. They pass-
ively attach to various receptors,
including complement receptors, on
the host cell surface by means of
lipophosphoglycan and gp63 and
are taken up by conventional
phagocytosis. Leishmania-conraining
phagosomes fuse effectively with
lysosomes, as shown by the presence
of lysosomal enzymes within the
parasitophorous vacuole (D. RusselI;
St Louis) and kinetic studies have
revealed that a constant supply of
lysosomal enzymes is likely to be
released into these vacuoles. The
Researchers interested in immunologi-
caJ aspects of bacterial, fungal, pro-
tozoan and helminthic infection are
too often kept apart by artificial sub-
ject boundaries. These barriers were
temporarily breached by arecent
workshop * in which the comp/ex in-
terplay between microbes and their
mammalian hosts were examined (rom
aglobai viewpoint. The role of T-cell
subsets and their products came under
dose scrutiny but the most forceful
image was that of the macrophage. As
host for infective agents, as modulator
of specific immune activity and as ulti-
mate mediator of the host response,
the macrophage plays a virtuoso's role
in the host-parasite drama.
magnitude of the respiratory burst
is decreased when triggered by
complement-coated parasites, so
that the mechanism of entry may
contribute in more than one way to
the survival of the parasite.
Macrophages as antigen-presenting
cells (APCs)
Two major pathways have
evolved for the presentation of anti-
gen to T cells. Intracellular antigens
are mainly processed in the cytosol
and are presented in the context of
MHC dass I molecules, whereas ex-
ogenous antigens are generally pro-
cessed by the endosomal pathway
and associate with MHC dass 11
molecules. P. Kaye (London), work-
ing with Leishmania donovani,
showed that phagolysosomes of
infected macrophages contain para-
sites in various stages of degra-
dation. Although MHC dass 11 mol-
ecules could be seen within the
phagolysosomes, they are not used
*The Fourth International Erlangen
Workshop on Moleeular Aspects of Im-
munological Host-Parasite Interactions
was held at Erlangen, FRG on 27-29
September 1990. It was organized by M.
Röllinghoff, W. Solbach and J. Kalden.
© 1991, Elsevier Scicnce Publishers Ltd, UK. 0167--4919/91/$02.00
Immunology Today 4 Vol. 12, No. 1 1991
for antigen presentation: the meta-
bolie inhibitor Brefeldin-A abro-
ga ted the presentation of parasite
antigens to MHC dass-II-restricted
T cells. Brefeldin-A blocks the trans-
port of newly synthesized proteins
from the endoplasmic reticulum to
the Golgi apparatus, suggesting that
only nascent MHC molecules are
used by APCs.
The macrophage as an APC plays
a key role in determining whether or
not a cellular immune response pro-
motes protection of the host or sur-
vival of the infectious agent. One
important factor is the level of ex-
pression of MHC molecuJes; as
an illustration of this, H-D. Volk
(Berlin) showed data demonstrating
that in patients with septicemia there
is a dose association between re-
duction in monocyte HLA-DR ex-
pression and fatal outcome.
MHC antigen expression is modu-
lated by T-cell-derived cytokines but
can also be profoundly influenced
by the natural resistance gene Beg
(which is probably identical to lty
and Lsh). Beg is located on mouse
chromosome 1 and, presumably, on
human chromosome 2q, within a set
of genes coding for cytoskeletal pro-
teins (E. Skarnene, Montreal). In its
two allelic forms Beg confers resist-
ance and susceptibility to infee-
tion with Salmonella typhimurium,
Leishmania donovani, mycobacteria
and other macrophagic parasites
in mice and preliminary studies in
humans suggest a similar dichot-
omy. The Beg gene product, in ad-
dition to controlling MHC dass 11
antigen expression, affects 5' nu-
deotidase activation, the respiratory
burst and expression of the ligand
for AcM.l, an antibody that recog-
nizes activated macrophagcs.
MHC molecules direct the im-
mune system towards responses me-
dia ted largely by either CD4 + or
CD8+ T cells and this may be partly