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J Biol Chem, Vol. 274, Issue 3, 1240-1247, January 15, 1999

A Requirement for Phosphatidylinositol 3-Kinase in Pseudopod Extension

Dianne Cox, Ching-Chun Tseng, Gordana Bjekic, and Steven Greenberg

From the Departments of Medicine and Pharmacology, Columbia University College of Physicians and Surgeons, New York, New York 10032

Phagocytosis requires actin assembly and pseudopod extension, two cellular events that coincide spatially and temporally. The signal transduction events underlying both processes may be distinct. We tested whether phagocytic signaling resembles that of growth factor receptors, which induce actin polymerization via activation of phosphatidylinositol 3-kinase (PI 3-kinase). Fcgamma receptor-mediated phagocytosis was accompanied by a rapid increase in the accumulation of phosphatidylinositol 3,4,5-trisphosphate in vivo, and addition of wortmannin (WM) or LY294002, two inhibitors of PI 3-kinase(s), inhibited phagocytosis but not Fcgamma receptor-directed actin polymerization. However, both compounds prevented maximal pseudopod extension, suggesting that PI 3-kinase inhibition produced a limitation in membrane required for pseudopod extension. Availability of plasma membrane was not limiting for phagocytosis, because blockade of ingestion in the presence of WM was not overcome by reducing the number of particles adhering to macrophages. However, decreasing bead size, and hence the magnitude of pseudopod extension required for particle engulfment, relieved the inhibition of phagocytosis in the presence of WM or LY294002 by up to 80%. The block in phagocytosis of large particles occurred before phagosomal closure, because both compounds inhibited spreading of macrophages on substrate-bound IgG. Macrophage spreading on IgG was accompanied by exocytic insertion of membrane from an intracellular source, as measured by the dye FM1-43. These results indicate that one or more isoforms of PI 3 kinase are required for maximal pseudopod extension but not phagocytosis per se. We suggest that PI 3-kinase is required for coordinating exocytic membrane insertion and pseudopod extension.


Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.
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P.-Y. Berclaz, Z. Zsengeller, Y. Shibata, K. Otake, S. Strasbaugh, J. A. Whitsett, and B. C. Trapnell
Endocytic Internalization of Adenovirus, Nonspecific Phagocytosis, and Cytoskeletal Organization Are Coordinately Regulated in Alveolar Macrophages by GM-CSF and PU.1
J. Immunol., December 1, 2002; 169(11): 6332 - 6342.
[Abstract] [Full Text] [PDF]


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BloodHome page
P.-Y. Berclaz, Y. Shibata, J. A. Whitsett, and B. C. Trapnell
GM-CSF, via PU.1, regulates alveolar macrophage Fcgamma R-mediated phagocytosis and the IL-18/IFN-gamma -mediated molecular connection between innate and adaptive immunity in the lung
Blood, December 1, 2002; 100(12): 4193 - 4200.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. G. Coppolino, R. Dierckman, J. Loijens, R. F. Collins, M. Pouladi, J. Jongstra-Bilen, A. D. Schreiber, W. S. Trimble, R. Anderson, and S. Grinstein
Inhibition of Phosphatidylinositol-4-phosphate 5-Kinase Ialpha Impairs Localized Actin Remodeling and Suppresses Phagocytosis
J. Biol. Chem., November 8, 2002; 277(46): 43849 - 43857.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
J. C. Edberg, H. Qin, A. W. Gibson, A. M. F. Yee, P. B. Redecha, Z. K. Indik, A. D. Schreiber, and R. P. Kimberly
The CY Domain of the Fcgamma RIa alpha -Chain (CD64) Alters gamma -Chain Tyrosine-based Signaling and Phagocytosis
J. Biol. Chem., October 18, 2002; 277(43): 41287 - 41293.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
E. Garcia-Garcia, R. Rosales, and C. Rosales
Phosphatidylinositol 3-kinase and extracellular signal-regulated kinase are recruited for Fc receptor-mediated phagocytosis during monocyte-to-macrophage differentiation
J. Leukoc. Biol., July 1, 2002; 72(1): 107 - 114.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
L.-A. H. Allen, C. Yang, and J. E. Pessin
Rate and extent of phagocytosis in macrophages lacking vamp3
J. Leukoc. Biol., July 1, 2002; 72(1): 217 - 221.
[Abstract] [Full Text] [PDF]


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JCBHome page
O. Barreiro, M. Yanez-Mo, J. M. Serrador, M. C. Montoya, M. Vicente-Manzanares, R. Tejedor, H. Furthmayr, and F. Sanchez-Madrid
Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes
J. Cell Biol., June 24, 2002; 157(7): 1233 - 1245.
[Abstract] [Full Text] [PDF]


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Am. J. Pathol.Home page
P. Maderna, D. C. Cottell, G. Berlasconi, N. A. Petasis, H. R. Brady, and C. Godson
Lipoxins Induce Actin Reorganization in Monocytes and Macrophages But Not in Neutrophils : Differential Involvement of Rho GTPases
Am. J. Pathol., June 1, 2002; 160(6): 2275 - 2283.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
S. D. Kobayashi, J. M. Voyich, C. L. Buhl, R. M. Stahl, and F. R. DeLeo
Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: Cell fate is regulated at the level of gene expression
PNAS, May 14, 2002; 99(10): 6901 - 6906.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
B. Hu, A. Punturieri, J. Todt, J. Sonstein, T. Polak, and J. L. Curtis
Recognition and phagocytosis of apoptotic T cells by resident murine tissue macrophages require multiple signal transduction events
J. Leukoc. Biol., May 1, 2002; 71(5): 881 - 889.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
P. P. Sanna, M. Cammalleri, F. Berton, C. Simpson, R. Lutjens, F. E. Bloom, and W. Francesconi
Phosphatidylinositol 3-Kinase Is Required for the Expression But Not for the Induction or the Maintenance of Long-Term Potentiation in the Hippocampal CA1 Region
J. Neurosci., May 1, 2002; 22(9): 3359 - 3365.
[Abstract] [Full Text] [PDF]


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Am. J. Pathol.Home page
A. K. McNally and J. M. Anderson
{beta}1 and {beta}2 Integrins Mediate Adhesion during Macrophage Fusion and Multinucleated Foreign Body Giant Cell Formation
Am. J. Pathol., February 1, 2002; 160(2): 621 - 630.
[Abstract] [Full Text] [PDF]


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BloodHome page
R. Wiewrodt, A. P. Thomas, L. Cipelletti, M. Christofidou-Solomidou, D. A. Weitz, S. I. Feinstein, D. Schaffer, S. M. Albelda, M. Koval, and V. R. Muzykantov
Size-dependent intracellular immunotargeting of therapeutic cargoes into endothelial cells
Blood, February 1, 2002; 99(3): 912 - 922.
[Abstract] [Full Text] [PDF]


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JCBHome page
O. V. Vieira, R. J. Botelho, L. Rameh, S. M. Brachmann, T. Matsuo, H. W. Davidson, A. Schreiber, J. M. Backer, L. C. Cantley, and S. Grinstein
Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation
J. Cell Biol., October 1, 2001; 155(1): 19 - 26.
[Abstract] [Full Text] [PDF]


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JCBHome page
J. G. Marshall, J. W. Booth, V. Stambolic, T. Mak, T. Balla, A. D. Schreiber, T. Meyer, and S. Grinstein
Restricted Accumulation of Phosphatidylinositol 3-Kinase Products in a Plasmalemmal Subdomain during Fc{gamma} Receptor-mediated Phagocytosis
J. Cell Biol., June 18, 2001; 153(7): 1369 - 1380.
[Abstract] [Full Text] [PDF]


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JEMHome page
H. Uchida, A. Kondo, Y. Yoshimura, Y. Mazaki, and H. Sabe
PAG3/Pap{{alpha}}/KIAA0400, a GTPase-activating Protein for ADP-Ribosylation Factor (ARF), Regulates ARF6 in Fc{{gamma}} Receptor-mediated Phagocytosis of Macrophages
J. Exp. Med., April 16, 2001; 193(8): 955 - 966.
[Abstract] [Full Text] [PDF]


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J. Cell Sci.Home page
M. G. Coppolino, M. Krause, P. Hagendorff, D. A. Monner, W. Trimble, S. Grinstein, J. Wehland, and A. S. Sechi
Evidence for a molecular complex consisting of Fyb/SLAP, SLP-76, Nck, VASP and WASP that links the actin cytoskeleton to Fc{gamma} receptor signalling during phagocytosis
J. Cell Sci., January 12, 2001; 114(23): 4307 - 4318.
[Abstract] [Full Text] [PDF]


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J. Cell Sci.Home page
A. Rupper, J. Rodriguez-Paris, B. Grove, and J. Cardelli
p110-related PI 3-kinases regulate phagosome-phagosome fusion and phagosomal pH through a PKB/Akt dependent pathway in Dictyostelium
J. Cell Sci., January 4, 2001; 114(7): 1283 - 1295.
[Abstract] [PDF]


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J. Cell Sci.Home page
R. May and L. Machesky
Phagocytosis and the actin cytoskeleton
J. Cell Sci., January 3, 2001; 114(6): 1061 - 1077.
[Abstract] [PDF]


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JEMHome page
D. Cox, B. M. Dale, M. Kashiwada, C. D. Helgason, and S. Greenberg
A Regulatory Role for Src Homology 2 Domain-containing Inositol 5'-Phosphatase (SHIP) in Phagocytosis Mediated by Fc{{gamma}} Receptors and Complement Receptor 3 ({{alpha}}M{beta}2; CD11b/CD18)
J. Exp. Med., December 27, 2000; 193(1): 61 - 72.
[Abstract] [Full Text] [PDF]


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JCBHome page
R. J. Botelho, M. Teruel, R. Dierckman, R. Anderson, A. Wells, J. D. York, T. Meyer, and S. Grinstein
Localized Biphasic Changes in Phosphatidylinositol-4,5-Bisphosphate at Sites of Phagocytosis
J. Cell Biol., December 18, 2000; 151(7): 1353 - 1368.
[Abstract] [Full Text] [PDF]


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Mol. Biol. CellHome page
M. Amyere, B. Payrastre, U. Krause, P. V. D. Smissen, A. Veithen, and P. J. Courtoy
Constitutive Macropinocytosis in Oncogene-transformed Fibroblasts Depends on Sequential Permanent Activation of Phosphoinositide 3-Kinase and Phospholipase C
Mol. Biol. Cell, October 1, 2000; 11(10): 3453 - 3467.
[Abstract] [Full Text]


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J. Immunol.Home page
L. Serrander, P. Skarman, B. Rasmussen, W. Witke, D. P. Lew, K.-H. Krause, O. Stendahl, and O. Nu{beta}e
Selective Inhibition of IgG-Mediated Phagocytosis in Gelsolin-Deficient Murine Neutrophils
J. Immunol., September 1, 2000; 165(5): 2451 - 2457.
[Abstract] [Full Text] [PDF]


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JCBHome page
L. Bajno, X.-R. Peng, A. D. Schreiber, H.-P. Moore, W. S. Trimble, and S. Grinstein
Focal Exocytosis of VAMP3-containing Vesicles at Sites of Phagosome Formation
J. Cell Biol., May 1, 2000; 149(3): 697 - 706.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. Emoto, J. K. Klarlund, S. B. Waters, V. Hu, J. M. Buxton, A. Chawla, and M. P. Czech
A Role for Phospholipase D in GLUT4 Glucose Transporter Translocation
J. Biol. Chem., March 15, 2000; 275(10): 7144 - 7151.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
D. J. Lee, D. Cox, J. Li, and S. Greenberg
Rac1 and Cdc42 Are Required for Phagocytosis, but Not NF-kappa B-dependent Gene Expression, in Macrophages Challenged with Pseudomonas aeruginosa
J. Biol. Chem., January 7, 2000; 275(1): 141 - 146.
[Abstract] [Full Text] [PDF]


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JEMHome page
E. S. Gold, D. M. Underhill, N. S. Morrissette, J. Guo, M. A. McNiven, and A. Aderem
Dynamin 2 Is Required for Phagocytosis in Macrophages
J. Exp. Med., December 20, 1999; 190(12): 1849 - 1856.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. G. Coppolino, C. Kong, M. Mohtashami, A. D. Schreiber, J. H. Brumell, B. B. Finlay, S. Grinstein, and W. S. Trimble
Requirement for N-Ethylmaleimide-sensitive Factor Activity at Different Stages of Bacterial Invasion and Phagocytosis
J. Biol. Chem., February 9, 2001; 276(7): 4772 - 4780.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
D. J. Hackam, R. J. Botelho, C. Sjolin, O. D. Rotstein, J. M. Robinson, A. D. Schreiber, and S. Grinstein
Indirect Role for COPI in the Completion of Fcgamma Receptor-mediated Phagocytosis
J. Biol. Chem., May 18, 2001; 276(21): 18200 - 18208.
[Abstract] [Full Text] [PDF]




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