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J. Biol. Chem., Vol. 278, Issue 5, 3331-3338, January 31, 2003
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From the Departments of Clustering of macrophage Fc
Differential Role of Actin, Clathrin, and Dynamin
in Fc
Receptor-mediated Endocytosis and Phagocytosis*
§¶
,,
Pediatrics, § Cell
Biology, and ¶¶ Medicine, ¶ Division of Rheumatology,
Hospital for Sick Children, Institute of Medical Science, and
University Health Network, University of Toronto, Toronto, Ontario
M5G 1X8, Canada, ** Department of Immunology, University of
Washington, Seattle, Washington 98195, Department of Medicine, University of
Pennsylvania School of Medicine, Philadelphia, Pennsylvania
19104-4283, and §§ Institute for Cancer
Research, The Norwegian Radium Hospital, Montebello, 0310 Oslo,
Norway
receptors by multimeric immunoglobulin complexes leads to their
internalization. Formation of small aggregates leads to endocytosis,
whereas large particulate complexes induce phagocytosis. In RAW-264.7
macrophages, Fc receptor endocytosis was found to be dependent on
clathrin and dynamin and insensitive to cytochalasin. Clathrin also
associates with nascent phagosomes, and earlier observations suggested
that it plays an essential role in phagosome formation. However, we
find that phagocytosis of IgG-coated large (
3 µm) particles was
unaffected by inhibition of dynamin or by reducing the expression of
clathrin using antisense mRNA but was eliminated by cytochalasin,
implying a distinct mechanism dependent on actin assembly. The uptake
of smaller particles (
1 µm) was only partially blocked by
cytochalasin. Remarkably, the cytochalasin-resistant component was also
insensitive to dominant-negative dynamin I and to clathrin antisense
mRNA, implying the existence of a third internalization mechanism,
independent of actin, dynamin, and clathrin. The uptake of small
particles occurred by a process distinct from fluid phase pinocytosis,
because it was not inhibited by dominant-negative Rab5. The
insensitivity of phagocytosis to dominant-negative dynamin I enabled us
to test the role of dynamin in phagosomal maturation. Although
internalization of receptors from the plasma membrane was virtually
eliminated by the K44A and S45N mutants of dynamin I, clearance of
transferrin receptors and of CD18 from maturing phagosomes was
unaffected by these mutants. This implies that removal of receptors
from the phagosomal membrane occurs by a mechanism that is different from the one mediating internalization of the same receptors at the
plasma membrane. These results imply that, contrary to prevailing notions, normal dynamin and clathrin function is not required for
phagocytosis and reveal the existence of a component of phagocytosis that is independent of actin and Rab5.
*
This work was supported in part by the Canadian Institutes
of Health Research (CIHR), the Arthritis Society of Canada, the Arthritis Center of Excellence, and the Sanatorium Foundation.The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Supported by a CIHR fellowship, the Arthritis Society of
Canada, and the Arthritis Center of Excellence.
Current holder of the Pitblado Chair in Cell Biology at
The Hospital for Sick Children. Cross-appointed to the Department of
Biochemistry, University of Toronto. To whom correspondence should be
addressed: Dept. of Cell Biology, Hospital for Sick Children, 555 University Ave., Toronto, Ontario M5G 1X8, Canada. Tel.: 416-813-5727;
Fax: 416-813-5028; E-mail: sga@sickkids.ca.
Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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