J. Biol. Chem., Vol. 261, Issue 14, 6408-6415, May, 1986
Matrix magnesium and the permeability of heart mitochondria to potassium ion
DW Jung and GP Brierley
Isolated beef heart mitochondria were treated with A23187 in the presence
of different concentrations of Mg2+ or EDTA to establish varying levels of
total mitochondrial Mg2+. The Mg2+ content was related to the rate of
passive swelling of the mitochondria in potassium acetate and other
potassium salts in which swelling is presumed to depend on K+ entry via an
endogenous K+/H+ antiport. Swelling in these salts does not commence until
Mg2+ has been depleted from an initial value of 36 nmol X mg-1 of protein
to 8 nmol/mg-1, or less. Below this level, swelling increases linearly with
decreasing Mg2+ to a maximum rate at 2 nmol of Mg2+ X mg-1.
Rotenone-treated heart mitochondria suspended in 75 mM potassium acetate at
pH 7.80 show no delta pH by 5,5-dimethyl-2,4-oxazolidinedione distribution.
Distribution of methylamine also shows essentially no delta pH under these
conditions when allowance is made for binding of [14C]methylamine by
mitochondrial membranes under these conditions. Addition of A23187 results
in a small and transient delta pH (delta pH less than 0.14, acid interior)
as measured by methylamine distribution. Estimation of the maximum matrix
free Mg2+ concentration from the maximum delta pH observed and the external
free Mg2+ concentration at equilibrium with A23187 shows that swelling is
not initiated until matrix free Mg2+ is decreased to below 150 microM. An
independent estimate of free Mg2+ using a null-point procedure gives a
lower, but quite similar value (50 microM) for maximum matrix free Mg2+
when swelling commences. The large depletion of total and free Mg2+ that is
required to activate swelling in potassium acetate (and presumably K+/H+
antiport activity) does not appear to be compatible with previous
indications that free Mg2+ acts as a "carrier brake" to regulate K+
extrusion from the mitochondrion on such an antiport (Garlid, K. D. (1980)
J. Biol. Chem. 255, 11273- 11279). The removal of a tightly bound component
of mitochondrial Mg2+ is closely related to increased K+ permeability and
increased passive swelling in potassium salts. This Mg2+ appears to play a
role in the maintenance of mitochondrial membrane structure and integrity.
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