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J Biol Chem, Vol. 274, Issue 16, 10983-10989, April 16, 1999
From the Phosphatidylinositol
3,4,5-trisphosphate (PI(3,4,5)P3) has been proposed
to act as a second messenger to recruit regulatory proteins to the
plasma membrane via their pleckstrin homology (PH) domains. The PH
domain of Bruton's tyrosine kinase (Btk), which is mutated in the
human disease X-linked agammaglobulinemia, has been shown to interact
with PI(3,4,5)P3 in vitro. In this study,
a fusion protein containing the PH domain of Btk and the enhanced green
fluorescent protein (BtkPH-GFP) was constructed and utilized to
study the ability of this PH domain to interact with membrane inositol
phospholipids inside living cells. The localization of expressed
BtkPH-GFP in quiescent NIH 3T3 cells was indistinguishable from that of
GFP alone, both being cytosolic as assessed by confocal microscopy. In
NIH 3T3 cells coexpressing BtkPH-GFP and the epidermal growth factor
receptor, activation of epidermal growth factor or endogenous
platelet-derived growth factor receptors caused a rapid (<3 min)
translocation of the cytosolic fluorescence to ruffle-like membrane
structures. This response was not observed in cells expressing GFP only
and was completely inhibited by treatment with the PI 3-kinase
inhibitors wortmannin and LY 292004. Membrane-targeted PI 3-kinase also
caused membrane localization of BtkPH-GFP that was slowly reversed by wortmannin. When the R28C mutation of the Btk PH domain, which causes
X-linked agammaglobulinemia, was introduced into the fluorescent construct, no translocation was observed after stimulation. In contrast, the E41K mutation, which confers transforming activity to
native Btk, caused significant membrane localization of BtkPH-GFP with
characteristics indicating its possible binding to
PI(4,5)P2. This mutant, but not wild-type BtkPH-GFP,
interfered with agonist-induced PI(4,5)P2 hydrolysis in
COS-7 cells. These results show in intact cells that the PH domain of
Btk binds selectively to 3-phosphorylated lipids after activation of PI
3-kinase enzymes and that losing such binding ability or specificity
results in gross abnormalities in the function of the enzyme.
Therefore, the interaction with PI(3,4,5)P3 is likely
to be an important determinant of the physiological regulation of Btk
and can be utilized to visualize the dynamics and spatiotemporal
organization of changes in this phospholipid in living cells.
Phosphatidylinositol 3-Kinase-dependent Membrane
Association of the Bruton's Tyrosine Kinase Pleckstrin Homology
Domain Visualized in Single Living Cells
,
Endocrinology and Reproduction Research
Branch and the § Developmental Endocrinology Branch,
NICHD, National Institutes of Health,
Bethesda, Maryland 20892-4510
Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.
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