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Gating Properties of Heterotypic Gap Junction Channels Formed of Connexins 40, 43, and 45

Mindaugas Rackauskas ^*, Maria M. Kreuzberg , Mindaugas Pranevicius , Klaus Willecke , Vytas K. Verselis ^* and Feliksas F. Bukauskas ^*

^* Department of Neuroscience and Department of Anesthesiology of Albert Einstein College of Medicine, Bronx, New York; and Institut für Genetik, Abteilung Molekulargenetik, Universität Bonn, Bonn, Germany

Correspondence: Address reprint requests to Dr. Feliksas F. Bukauskas, 1300 Morris Park Ave., Albert Einstein College of Medicine, Bronx, NY 10461. Tel.: 718-430-4130; Fax: 718-430-8944; E-mail: fbukausk{at}aecom.yu.edu.

Connexins (Cxs) 40, 43, and 45 are expressed in many different tissues, but most abundantly in the heart, blood vessels, and the nervous system. We examined formation and gating properties of heterotypic gap junction (GJ) channels assembled between cells expressing wild-type Cx40, Cx43, or Cx45 and their fusion forms tagged with color variants of green fluorescent protein. We show that these Cxs, with exception of Cxs 40 and 43, are compatible to form functional heterotypic GJ channels. Cx40 and Cx43 hemichannels are unable or effectively impaired in their ability to dock and/or assemble into junctional plaques. When cells expressing Cx45 contacted those expressing Cx40 or Cx43 they readily formed junctional plaques with cell-cell coupling characterized by asymmetric junctional conductance dependence on transjunctional voltage, V_j. Cx40/Cx45 heterotypic GJ channels preferentially exhibit V_j-dependent gating transitions between open and residual states with a conductance of 42 pS; transitions between fully open and closed states with conductance of 52 pS in magnitude occur at substantially lower (10-fold) frequency. Cx40/Cx45 junctions demonstrate electrical signal transfer asymmetry that can be modulated between unidirectional and bidirectional by small changes in the difference between holding potentials of the coupled cells. Furthermore, both fast and slow gating mechanisms of Cx40 exhibit a negative gating polarity.

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