Evidence for Direct Physical Association between a K+ Channel (Kir6.2) and an ATP-Binding Cassette Protein (SUR1) Which Affects Cellular Distribution and Kinetic Behavior of an ATP-Sensitive K+ Channel

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Mol Cell Biol, March 1998, p. 1652-1659, Vol. 18, No. 3
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Evidence for Direct Physical Association between a K⁺ Channel (Kir6.2) and an ATP-Binding Cassette Protein (SUR1) Which Affects Cellular Distribution and Kinetic Behavior of an ATP-Sensitive K⁺ Channel

Eva Lorenz,¹ Alexey E. Alekseev,¹ Grigory B. Krapivinsky,² Antonio J. Carrasco,¹ David E. Clapham,² and Andre Terzic¹^,^*

Departments of Medicine and Pharmacology, Division of Cardiovascular Diseases, Mayo Clinic, Mayo Foundation, Rochester, Minnesota 55905,¹ and Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts 02115²

Received 10 October 1997/Returned for modification 24 November 1997/Accepted 12 December 1997

Structurally unique among ion channels, ATP-sensitive K⁺ (K_ATP) channels are essential in coupling cellular metabolism withmembrane excitability, and their activity can be reconstitutedby coexpression of an inwardly rectifying K⁺ channel, Kir6.2, with an ATP-binding cassette protein, SUR1.To determine if constitutive channel subunits form a physicalcomplex, we developed antibodies to specifically label and immunoprecipitateKir6.2. From a mixture of Kir6.2 and SUR1 in vitro-translatedproteins, and from COS cells transfected with both channel subunits,the Kir6.2-specific antibody coimmunoprecipitated 38- and 140-kDaproteins corresponding to Kir6.2 and SUR1, respectively. Sinceprevious reports suggest that the carboxy-truncated Kir6.2 canform a channel independent of SUR, we deleted 114 nucleotidesfrom the carboxy terminus of the Kir6.2 open reading frame (Kir6.2 $Delta$ C37).Kir6.2 $Delta$ C37 still coimmunoprecipitated with SUR1, suggesting thatthe distal carboxy terminus of Kir6.2 is unnecessary for subunitassociation. Confocal microscopic images of COS cells transfectedwith Kir6.2 or Kir6.2 $Delta$ C37 and labeled with fluorescent antibodiesrevealed unique honeycomb patterns unlike the diffuse immunostainingobserved when cells were cotransfected with Kir6.2-SUR1 or Kir6.2 $Delta$ C37-SUR1.Membrane patches excised from COS cells cotransfected with Kir6.2-SUR1or Kir6.2 $Delta$ C37-SUR1 exhibited single-channel activity characteristicof pancreatic K_ATP channels. Kir6.2 $Delta$ C37 alone formed functionalchannels with single-channel conductance and intraburst kineticproperties similar to those of Kir6.2-SUR1 or Kir6.2 $Delta$ C37-SUR1but with reduced burst duration. This study provides direct evidencethat an inwardly rectifying K⁺ channel and an ATP-binding cassette protein physically associate,which affects the cellular distribution and kinetic behavior ofa K_ATP channel.

^* Corresponding author. Mailing address: Guggenheim 7, Mayo Clinic, Rochester, MN 55905. Phone: (507) 284-2747. Fax: (507) 284-9111.E-mail: terzic.andre{at}mayo.edu.

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