Localized Biphasic Changes in Phosphatidylinositol-4,5-Bisphosphate at Sites of Phagocytosis

doi:10.1083/jcb.151.7.1353

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Published online 18 December 2000. doi:10.1083/jcb.151.7.1353

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© The Rockefeller University Press, 0021-9525/2000/12/1353/ $5.00
The Journal of Cell Biology, Volume 151, Number 7, December 25, 2000 1353-1368

Original Article

Localized Biphasic Changes in Phosphatidylinositol-4,5-Bisphosphate at Sites of Phagocytosis

Roberto J. Botelho^a, Mary Teruel^e, Renee Dierckman^b, Richard Anderson^b, Alan Wells^c, John D. York^d, Tobias Meyer^e, and Sergio Grinstein^a
^a Cell Biology Program, Hospital for Sick Children, and Department of Biochemistry, University of Toronto, Ontario M5G 1X8, Canada
^b Department of Pharmacology, University of Wisconsin School of Medicine, Madison, Wisconsin 53706
^c Department of Pathology, University of Pittsburgh, Pittsburgh, Pennsylvania 15261
^d Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, North Carolina 27710
^e Department of Cell Biology, Duke University Medical Center, Durham, North Carolina 27710

Correspondence to: Sergio Grinstein, Hospital for Sick Children, Division of Cell Biology, 555 University Ave., Toronto, Ontario M5G 1X8, Canada. Tel:(416) 813-5727 Fax:(416) 813-5028 E-mail:sga{at}sickkids.on.ca.

Phagocytosis requires localized and transient remodeling ofactin filaments. Phosphoinositide signaling is believed to playan important role in cytoskeletal organization, but it is unclearwhether lipids, which can diffuse along the membrane, can mediatethe focal actin assembly required for phagocytosis. We usedimaging of fluorescent chimeras of pleckstrin homology and C1domains in live macrophages to monitor the distribution of phosphatidylinositol-4,5-bisphosphate(4,5-PIP₂) and diacylglycerol, respectively, during phagocytosis.Our results reveal a sequence of exquisitely localized, coordinatedsteps in phospholipid metabolism: a focal, rapid accumulationof 4,5-PIP₂ accompanied by recruitment of type I ${alpha}$ phosphatidylinositolphosphate kinase to the phagosomal cup, followed by disappearanceof the phosphoinositide as the phagosome seals. Loss of 4,5-PIP₂correlated with mobilization of phospholipase C ${gamma}$ (PLC ${gamma}$ ) and withthe localized formation of diacylglycerol. The presence of 4,5-PIP₂and active PLC ${gamma}$ at the phagosome was shown to be essential foreffective particle ingestion. The temporal sequence of phosphoinositidemetabolism suggests that accumulation of 4,5-PIP₂ is involvedin the initial recruitment of actin to the phagocytic cup, whileits degradation contributes to the subsequent cytoskeletal remodeling.

Key Words: Fc ${gamma}$ receptors, phospholipase C, PH domain, diacylglycerol, phosphatidylinositol

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Rozenvayn, N., Flaumenhaft, R. (2003). Protein kinase C Mediates Translocation of Type II Phosphatidylinositol 5-Phosphate 4-Kinase Required for Platelet alpha -Granule Secretion. J. Biol. Chem. 278: 8126-8134 [Abstract] [Full Text]
Araki, N., Hatae, T., Furukawa, A., Swanson, J. A. (2003). Phosphoinositide-3-kinase-independent contractile activities associated with Fc{gamma}-receptor-mediated phagocytosis and macropinocytosis in macrophages. J. Cell Sci. 116: 247-257 [Abstract] [Full Text]
Garcia-Garcia, E., Rosales, C. (2002). Signal transduction during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 72: 1092-1108 [Abstract] [Full Text]
Coppolino, M. G., Dierckman, R., Loijens, J., Collins, R. F., Pouladi, M., Jongstra-Bilen, J., Schreiber, A. D., Trimble, W. S., Anderson, R., Grinstein, S. (2002). Inhibition of Phosphatidylinositol-4-phosphate 5-Kinase Ialpha Impairs Localized Actin Remodeling and Suppresses Phagocytosis. J. Biol. Chem. 277: 43849-43857 [Abstract] [Full Text]
Botelho, R. J., Tapper, H., Furuya, W., Mojdami, D., Grinstein, S. (2002). Fc{gamma}R-Mediated Phagocytosis Stimulates Localized Pinocytosis in Human Neutrophils. J. Immunol. 169: 4423-4429 [Abstract] [Full Text]
Wang, J., Gambhir, A., Hangyas-Mihalyne, G., Murray, D., Golebiewska, U., McLaughlin, S. (2002). Lateral Sequestration of Phosphatidylinositol 4,5-Bisphosphate by the Basic Effector Domain of Myristoylated Alanine-rich C Kinase Substrate Is Due to Nonspecific Electrostatic Interactions. J. Biol. Chem. 277: 34401-34412 [Abstract] [Full Text]
van Rheenen, J., Jalink, K. (2002). Agonist-induced PIP2 Hydrolysis Inhibits Cortical Actin Dynamics: Regulation at a Global but not at a Micrometer Scale. Mol. Biol. Cell 13: 3257-3267 [Abstract] [Full Text]
Tanimura, A., Nezu, A., Morita, T., Hashimoto, N., Tojyo, Y. (2002). Interplay between Calcium, Diacylglycerol, and Phosphorylation in the Spatial and Temporal Regulation of PKCalpha -GFP. J. Biol. Chem. 277: 29054-29062 [Abstract] [Full Text]
Cho, H., Hwang, J.-Y., Kim, D., Shin, H.-S., Kim, Y., Earm, Y. E., Ho, W.-K. (2002). Acetylcholine-induced Phosphatidylinositol 4,5-Bisphosphate Depletion Does Not Cause Short-term Desensitization of G Protein-gated Inwardly Rectifying K+ Current in Mouse Atrial Myocytes. J. Biol. Chem. 277: 27742-27747 [Abstract] [Full Text]
Grimmer, S., van Deurs, B., Sandvig, K. (2002). Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J. Cell Sci. 115: 2953-2962 [Abstract] [Full Text]
Nasuhoglu, C., Feng, S., Mao, Y., Shammat, I., Yamamato, M., Earnest, S., Lemmon, M., Hilgemann, D. W. (2002). Modulation of cardiac PIP2 by cardioactive hormones and other physiologically relevant interventions. Am. J. Physiol. Cell Physiol. 283: C223-C234 [Abstract] [Full Text]
Barreiro, O., Yanez-Mo, M., Serrador, J. M., Montoya, M. C., Vicente-Manzanares, M., Tejedor, R., Furthmayr, H., Sanchez-Madrid, F. (2002). Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J. Cell Biol. 157: 1233-1245 [Abstract] [Full Text]
Hellsten, E., Bernard, D. J., Owens, J. W., Eckhaus, M., Suchy, S. F., Nussbaum, R. L. (2002). Sertoli Cell Vacuolization and Abnormal Germ Cell Adhesion in Mice Deficient in an Inositol Polyphosphate 5-Phosphatase. Biol. Reprod. 66: 1522-1530 [Abstract] [Full Text]
Ellson, C. D., Andrews, S., Stephens, L. R., Hawkins, P. T. (2002). The PX domain: a new phosphoinositide-binding module. J. Cell Sci. 115: 1099-1105 [Abstract] [Full Text]
Beningo, K. A., Wang, Y.-l. (2002). Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J. Cell Sci. 115: 849-856 [Abstract] [Full Text]
Hilgemann, D. W., Feng, S., Nasuhoglu, C. (2001). The Complex and Intriguing Lives of PIP2 with Ion Channels and Transporters. Sci Signal 2001: re19-re19 [Abstract] [Full Text]
Sato, T. K., Overduin, M., Emr, S. D. (2001). Location, Location, Location: Membrane Targeting Directed by PX Domains. Science 294: 1881-1885 [Abstract] [Full Text]
Brown, F. D., Rozelle, A. L., Yin, H. L., Balla, T., Donaldson, J. G. (2001). Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 154: 1007-1018 [Abstract] [Full Text]
Micheva, K. D., Holz, R. W., Smith, S. J. (2001). Regulation of presynaptic phosphatidylinositol 4,5-biphosphate by neuronal activity. J. Cell Biol. 154: 355-368 [Abstract] [Full Text]
Marshall, J. G., Booth, J. W., Stambolic, V., Mak, T., Balla, T., Schreiber, A. D., Meyer, T., Grinstein, S. (2001). Restricted Accumulation of Phosphatidylinositol 3-Kinase Products in a Plasmalemmal Subdomain during Fc{gamma} Receptor-mediated Phagocytosis. J. Cell Biol. 153: 1369-1380 [Abstract] [Full Text]
May, R., Machesky, L. (2001). Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114: 1061-1077 [Abstract]
Diakonova, M., Bokoch, G., Swanson, J. A. (2002). Dynamics of Cytoskeletal Proteins during Fcgamma Receptor-mediated Phagocytosis in Macrophages. Mol. Biol. Cell 13: 402-411 [Abstract] [Full Text]
Stefan, C. J., Audhya, A., Emr, S. D. (2002). The Yeast Synaptojanin-like Proteins Control the Cellular Distribution of Phosphatidylinositol (4,5)-Bisphosphate. Mol. Biol. Cell 13: 542-557 [Abstract] [Full Text]