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Originally published In Press as doi:10.1074/jbc.M203954200 on July 3, 2002

J. Biol. Chem., Vol. 277, Issue 37, 34401-34412, September 13, 2002
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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*

Jiyao WangDagger , Alok Gambhir§, Gyöngyi Hangyás-MihálynéDagger , Diana Murray, Urszula GolebiewskaDagger , and Stuart McLaughlinDagger ||

From the Dagger  Department of Physiology and Biophysics and the § Department of Physics and Astronomy, State University of New York, Stony Brook, New York 11794-8661 and the  Department of Microbiology and Immunology, Weill Medical College of Cornell University, New York, New York 10021

A peptide corresponding to the basic (+13), unstructured effector domain of myristoylated alanine-rich C kinase substrate (MARCKS) binds strongly to membranes containing phosphatidylinositol 4,5-bisphosphate (PIP2). Although aromatic residues contribute to the binding, three experiments suggest the binding is driven mainly by nonspecific local electrostatic interactions. First, peptides with 13 basic residues, Lys-13 and Arg-13, bind to PIP2-containing vesicles with the same high affinity as the effector domain peptide. Second, removing basic residues from the effector domain peptide reduces the binding energy by an amount that correlates with the number of charges removed. Third, peptides corresponding to a basic region in GAP43 and MARCKS effector domain-like regions in other proteins (e.g. MacMARCKS, adducin, Drosophila A kinase anchor protein 200, and N-methyl-D-aspartate receptor) also bind with an energy that correlates with the number of basic residues. Kinetic measurements suggest the effector domain binds to several PIP2. Theoretical calculations show the effector domain produces a local positive potential, even when bound to a bilayer with 33% monovalent acidic lipids, and should thus sequester PIP2 laterally. This electrostatic sequestration was observed experimentally using a phospholipase C assay. Our results are consistent with the hypothesis that MARCKS could reversibly sequester much of the PIP2 in the plasma membrane.

* This work was supported by National Institutes of Health Grant GM24971 and National Science Foundation Grant MCB9729538 (to S. M.).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.

|| To whom correspondence should be addressed: Dept. of Physiology and Biophysics, HSC, SUNY, Stony Brook, NY 11794-8661. Tel.: 631-444-3615; Fax: 631-444-3432; E-mail: smcl@epo.som.sunysb.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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