The properties and function of large conductance calcium- and voltage- activated potassium (BK) channels are modified by the tissue specific expression of regulatory β 1-subunits. Although the short cytosolic N-terminal domain of the β 1-subunit is important for controlling both BK channel trafficking and function, whether the same, or different, regions of the N-terminus control these distinct processes remain unknown. Here we demonstrate that the first six N-terminal residues, including K3, K4 and L5, are critical for controlling functional regulation, but not trafficking, of BK channels. This membrane distal region has features of an amphipathic helix that is predicted to control the orientation of the first transmembrane segment (TM1) of the β 1-subunit. In contrast, a membrane proximal leucine residue (L17) controls trafficking without affecting functional coupling, an effect that is in part dependent on controlling efficient ER exit of the pore-forming α-subunit. Thus cell surface trafficking and functional coupling with BK channels are controlled by distinct domains of the β 1-subunit N-terminus.
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