Journal of Leukocyte Biology
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Originally published online as doi:10.1189/jlb.0205091 on April 4, 2005

Published online before print April 4, 2005
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(Journal of Leukocyte Biology. 2005;78:220-230.)
© 2005 by Society for Leukocyte Biology

Phosphoinositide3-kinase regulates actin polymerization during delayed phagocytosis of Helicobacter pylori

Lee-Ann H. Allen1, J. Aaron Allgood2, Xuemei Han and Lara M. Wittine3

Department of Medicine and the Inflammation Program, University of Iowa and the VA Medical Center, Iowa City

1 Correspondence: Inflammation Program, University of Iowa, 2501 Crosspark Rd., MTF D154, Coralville, IA 52241. E-mail: lee-ann-allen{at}uiowa.edu

We have shown previously that ulcerogenic (type I) strains of Helicobacter pylori (Hp) retard their entry into macrophages. However, the signaling pathways that regulate Hp phagocytosis are largely undefined. We show here that Hp strongly activated class IA phosphoinositide3-kinases (PI3Ks) in macrophages, coincident with phagocytosis, and endogenous p85 and active protein kinase B{alpha} accumulated on forming phagosomes. PI3K inhibitors, wortmannin and LY294002, inhibited phagocytosis of Hp in a dose-dependent manner, and blockade of engulfment correlated directly with loss of 3'-phosphoinositides in the membrane subjacent to attached bacteria. During uptake of large immunoglobulin G (IgG)-coated particles, PI3Ks regulate pseudopod extension and phagosome closure. In marked contrast, we show here that 3'-phosphoinositides regulated actin polymerization at sites of Hp uptake. Moreover, Hp and IgG beads activated distinct PI3K isoforms. Phagosomes containing IgG-coated particles accumulated 3'-phosphatase and tensin homologue deleted on chromosome 10 and Src homology 2 domain-containing inositol 5'-phosphatase, yet Hp phagosomes did not. Finally, rapid uptake of IgG-opsonized Hp or a less-virulent type II Hp was PI3K-independent. We conclude that Hp and IgG beads are ingested by distinct mechanisms and that PI3Ks regulate the actin cytoskeleton during slow phagocytosis of ulcerogenic Hp.

Key Words: macrophage • signal transduction • phagosome




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