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Papers In Press, published online ahead of print August 28, 2002
J. Biol. Chem, 10.1074/jbc.M205386200
Submitted on May 31, 2002
Revised on August 26, 2002
Accepted on August 28, 2002

Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes

Thomas Nebl, Kersi N. Pestonjamasp, John D. Leszyk, Jessica L. Crowley, Sang W. Oh, and Elizabeth J. Luna

Department of Cell Biology, University of Massachusetts Medical School, Worcester, MA 01605

Corresponding Author: Elizabeth.Luna{at}umassmed.edu

Plasma membranes are organized into functional domains both by liquid-ordered packing into ‘lipid rafts’, structures that resist Triton extraction, and by attachments to underlying cytoskeletal proteins in assemblies called ‘membrane skeletons’. Although the actin cytoskeleton is implicated in many lipid raft-mediated signaling processes, little is known about the biochemical basis for actin involvement. We show here that a subset of plasma membrane skeleton proteins from bovine neutrophils co-isolates with cholesterol-rich, detergent-resistant membrane fragments (DRMs) that exhibit a relatively high buoyant density in sucrose (DRM-H; d ~ 1.16g/ml). Using MALDI-TOF and tandem mass spectrometry, we identified 19 major DRM-H proteins. Membrane skeleton proteins include fodrin (nonerythroid spectrin), myosin-IIA, myosin-IG, a-actinin 1, a-actinin 4, vimentin, and the F-actin binding protein, supervillin. Other DRM-H components include lipid raft-associated integral membrane proteins (stomatin, flotillin 1, flotillin 2), extracellular surface-bound and GPI-anchored proteins (IgM, membrane-type 6 matrix metalloproteinase), and intracellular dually acylated signaling proteins (Lyn kinase, Gai-2). Consistent with cytoskeletal association, most DRM-H associated flotillin 2, Lyn, and Gai-2 also resist extraction with 0.1 M octylglucoside. Supervillin, myosin-IG, and myosin-IIA resist extraction with 0.1 M sodium carbonate, a treatment that removes all detectable actin, suggesting that these cytoskeletal proteins are proximal to the DRM-H bilayer. Binding of supervillin to the DRM-H fragments is confirmed by co-immunoaffinity purification. In spreading neutrophils, supervillin localizes with F-actin in cell extensions and in discrete basal punctae that partially overlap with Gai staining. We suggest that the DRM-H fraction represents a membrane skeleton-associated subset of leukocyte signaling domains.


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