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M310365200v1
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Papers In Press, published online ahead of print October 30, 2003
J. Biol. Chem, 10.1074/jbc.M310365200
Submitted on September 18, 2003
Revised on October 29, 2003
Accepted on October 30, 2003

Plasma membrane-cytoskeleton-endoplasmic reticulum complexes in neurons and astrocytes

Lubomira Lencesova, Andrea O'Neill, Wendy G. Resneck, Robert J. Bloch, and Mordecai P. Blaustein

Department of Physiology, University of Maryland, Baltimore, MD 21201

Corresponding Author: mblauste{at}umaryland.edu

The possibility that certain integral plasma membrane (PM) proteins involved in Ca2+ homeostasis form junctional units with adjacent endoplasmic reticulum (ER) in neurons and glia was explored using immunoprecipitation (IP) and immunocytochemistry. Rat brain membranes were solubilized with the mild, non-ionic detergent, IGEPAL CA-630. Na+/Ca2+ exchanger type 1 (NCX1), a key PM Ca2+ transporter, was immunoprecipitated from the detergent-soluble fraction. Several abundant PM proteins co-immunoprecipitated with NCX1, including the alpha 2 and alpha 3 isoforms of the Na+ pump catalytic (alpha ) subunit, and the alpha 2 subunit of the dihydropyridine receptor. The adaptor protein, ankyrin 2 (Ank 2), and the cytoskeletal proteins, alpha -fodrin and beta -spectrin also selectively co-immunoprecipitated with NCX1, as did the ER proteins, Ca2+ pump type 2 (SERCA 2), and inositol-trisphosphate receptor type 1 (IP3R-1). In contrast, a number of other abundant PM, adaptor and cytoskeletal proteins did not co-IP with NCX1, including the Na+ pump alpha 1 isoform, PM Ca2+ pump type 1 (PMCA1), beta -fodrin, and Ank 3. In reciprocal experiments, IP with antibodies to the Na+ pump alpha 2 and alpha 3 isoforms, but not alpha 1, co-immunoprecipitated NCX1; the antibodies to alpha 1 did, however, co-IP PMCA1. Antibodies to Ank 2, alpha -fodrin, beta -spectrin and IP3R-1 all co-immunoprecipitated NCX1. Immunocytochemistry revealed partial co-localization of beta -spectrin with NCX1, Na+ pump alpha 3 and IP3R-1 in neurons, and of alpha -fodrin with NCX1 and SERCA2 in astrocytes. The data support the idea that, in neurons and glia, PM microdomains containing NCX1 and Na+ pumps with alpha 2 or alpha 3 subunits form Ca2+ signaling complexes with underlying ER containing SERCA2 and IP3R-1. These PM and ER components appear to be linked through the cytoskeletal spectrin network, to which they are probably tethered by Ank 2.


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