Deubiquitylating enzyme USP2 counteracts Nedd4-2-mediated downregulation of KCNQ1 potassium channels

Katarzyna Krzystanek, Hanne Borger Rasmussen, Morten Grunnet, Olivier Staub, Søren-Peter Olesen, Hugues Abriel, Thomas Jespersen

23 Citations (Scopus)

Abstract

Background: KCNQ1 (Kv7.1), together with its KCNE β subunits, plays a pivotal role both in the repolarization of cardiac tissue and in water and salt transport across epithelial membranes. Nedd4/Nedd4-like (neuronal precursor cellexpressed developmentally downregulated 4) ubiquitinprotein ligases interact with the KCNQ1 potassium channel through a PY motif located in the C terminus of KCNQ1. This interaction induces ubiquitylation of KCNQ1, resulting in a reduced surface density of the channel. It was reported recently that the epithelial sodium channel is regulated by the reverse process-deubiquitylation- mediated by USP2 (ubiquitin-specific protease 2). Objective: In this article, we investigated whether deubiquitylation may regulate KCNQ1 channel complexes. Methods: In this study, we used electrophysiology, biochemistry, and confocal microscopy. Results: Electrophysiological investigations of KCNQ1/KCNE1 proteins coexpressed with USP2-45 or USP2-69 isoforms and Nedd4-2 in Xenopus laevis oocytes and mammalian cells revealed that both USP2 isoforms counter the Nedd4-2specific downregulation of IKs. Biochemical studies showed that the total and surface-expressed KCNQ1 protein was more abundant when coexpressed with USP2 and Nedd4-2 as compared with Nedd4-2 alone. Western blotting revealed partial protection against covalent attachment of ubiquitin moieties on KCNQ1 when USP2 was coexpressed with Nedd4-2. Coimmunoprecipitation assays suggested that USP2 can bind to KCNQ1 independently of the PY motif. Immunocytochemistry confirmed that USP2 restores the membrane localization of KCNQ1. Conclusion: These results demonstrate that USP2 can be a potent regulator of KCNQ1 surface density. USP2, which is well expressed in many tissues, may therefore be important in controlling the KCNQ1 channel dynamics in vivo.

Original languageEnglish
JournalHeart Rhythm
Volume9
Issue number3
Pages (from-to)440-8
Number of pages9
ISSN1547-5271
DOIs
Publication statusPublished - Mar 2012

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