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R-Mediated Phagocytosis Stimulates Localized Pinocytosis in Human Neutrophils1
* Program in Cell Biology, Hospital for Sick Children, and Department of Biochemistry, University of Toronto, Toronto, Ontario, Canada; and
Department of Cell and Molecular Biology, Section for Molecular Pathogenesis, Lund University, Lund, Sweden
Engulfment of IgG-coated particles by neutrophils and macrophages
is an essential component of the innate immune response. This process,
known as phagocytosis, is triggered by clustering of Fc
R at sites
where leukocytes make contact with the opsonized particles. We found
that phagocytosis is accompanied by a burst of fluid phase pinocytosis,
which is largely restricted to the immediate vicinity of the phagosomal
cup. FcR-induced pinocytosis preceded and appeared to be independent
of phagosomal sealing. Accordingly, fluid phase uptake was accentuated
by actin depolymerization, which precludes phagocytosis. Stimulation of
pinocytosis required phosphatidylinositol 3-kinase activity and was
eliminated when changes in the cytosolic free Ca2+
concentration were prevented. Because stimulation of FcR also
induces secretion, which is similarly calcium and phosphatidylinositol
3-kinase dependent, we studied the possible relationship between these
events. Neutrophil fragments devoid of secretory granules (cytoplasts)
were prepared by sedimentation through Ficoll gradients. Cytoplasts
could perform FcR-mediated phagocytosis, which was not accompanied
by activation of pinocytosis. This observation suggests that granule
exocytosis is required for stimulation of pinocytosis. Analysis of the
cytosolic Ca2+ dependence of secretion and pinocytosis
suggests that primary (lysosomal) granule exocytosis is the main
determinant of pinocytosis during FcR stimulation. Importantly,
primary granules are secreted in a polarized fashion near forming
phagosomes. Focal pinocytosis during particle engulfment may contribute
to Ag processing and presentation and/or to retrieval of components of
the secretory machinery. Alternatively, it may represent an early event
in the remodeling of the phagosomal membrane, leading to
phagosomal maturation.
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