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Opening Hemichannels in Nonjunctional Membrane Stimulates Gap Junction Formation

Department of Physiology and Biophysics, University of California at Irvine, Irvine, California

Correspondence: Address reprint requests to James E. Hall, Tel.: 949-824-5835; Fax: 949-824-3143; E-mail: jhall{at}uci.edu.

We studied gap junction formation in pairs of Xenopus laevis oocytes expressing connexins that form functional hemichannels and found no correlation between junctional conductance (G_j) and whole-cell hemichannel conductances (G_hemi) within the first few hours of pairing. However, opening hemichannels to a threshold current stimulated a rapid G_j increase. Moreover, cx46 hemichannel current stimulated cx40 G_j even though cx40 and cx46 do not form heteromeric or heterotypic gap junctions. Initial growth rate and final steady-state level of stimulated G_j were proportional to the product of hemichannel conductances. External calcium affected the growth rate of stimulated G_j but not the final steady-state value. Time constants of formation were short in low [Ca²⁺]_out (3 min in 200 µM Ca²⁺) and long in high [Ca²⁺]_out (15 min in 1 mM Ca²⁺), but in oocyte pairs pretreated with lectins to reduce steric hindrance imposed by large membrane glycoproteins the time constant was short and Ca²⁺-independent. We suggest that hemichannel activity stimulates G_j by collapsing the extracellular volume between membranes to allow the end-to-end binding between hemichannels. These studies suggest the possibility that functional hemichannels could trigger or enhance junctional formation in vivo in response to appropriate stimuli.