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Originally published In Press as doi:10.1074/jbc.M910068199 on March 15, 2000

J. Biol. Chem., Vol. 275, Issue 21, 15717-15727, May 26, 2000
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Role of COPI in Phagosome Maturation*

Roberto J. BotelhoDagger §, David J. HackamDagger , Alan D. Schreiber, and Sergio GrinsteinDagger ||

From the Dagger  Programme in Cell Biology, Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada and Department of Biochemistry of the University of Toronto, Toronto, Ontario M5G 1X8, Canada and the  Department of Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-4283

Phagosomes mature by sequentially fusing with endosomes and lysosomes. Vesicle budding is presumed to occur concomitantly, mediating the retrieval of plasmalemmal components and the regulation of phagosomal size. We analyzed whether fission of vesicles from phagosomes requires COPI, a multimeric complex known to be involved in budding from the Golgi and endosomes. The role of COPI was studied using ldlF cells, that harbor a temperature-sensitive mutation in epsilon -COP, a subunit of the coatomer complex. These cells were made phagocytic toward IgG-opsonized particles by heterologous expression of human Fcgamma RIIA receptors. Following incubation at the restrictive temperature, epsilon -COP was degraded in these cells and their Golgi complex dispersed. Nevertheless, phagocytosis persisted for hours in cells devoid of epsilon -COP. Retrieval of transferrin receptors from phagosomes became inefficient in the absence of epsilon -COP, while clearance of the Fcgamma RIIA receptors was unaffected. This indicates that fission of vesicles from the phagosomal membrane involves at least two mechanisms, one of which requires intact COPI. Traffic of fluid-phase markers and aggregated IgG-receptor complexes along the endocytic pathway was abnormal in epsilon -COP-deficient cells. In contrast, phagosome fusion with endosomes and lysosomes was unimpaired. Moreover, the resulting phagolysosomes were highly acidic. Similar results were obtained in RAW264.7 macrophages treated with brefeldin A, which precludes COPI assembly by interfering with the activation of adenosine ribosylation factor. These data indicate that neither phagosome formation nor maturation are absolutely dependent on COPI. Our findings imply that phagosomal maturation differs from endosomal progression, which appears to be more dependent on COPI-mediated formation of carrier vesicles.

* This work was supported in part by the Medical Research Council of Canada, the National Sanatorium Association, and National Institutes of Health Grant AI-22193.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.

§ Recipient of a Studentship from the Natural Sciences and Engineering Research Council of Canada.

|| International Scholar of the Howard Hughes Medical Institute and current holder of the Pitblado Chair in Cell Biology. To whom correspondence should be addressed: Div. of Cell Biology, 555 University Ave., Toronto M5G 1X8, Canada. Tel.: 416-813-5727; Fax: 416-813-5028; E-mail: sga@sickkids.on.ca.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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