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J Biol Chem, Vol. 274, Issue 19, 13281-13291, May 7, 1999

Glucose Generates Sub-plasma Membrane ATP Microdomains in Single Islet -Cells
POTENTIAL ROLE FOR STRATEGICALLY LOCATED MITOCHONDRIA

From the Department of Biochemistry, School of Medical Sciences, University of Bristol, Bristol BS8 1TD, United Kingdom and the ^§ Department of Biomedical Sciences and CNR Centre for Study of Biological Membranes, University of Padova, Via Trieste 75, 35121 Padua 17, Italy

Increases in the concentration of free ATP within the islet -cell may couple elevations in blood glucose to insulin release by closing ATP-sensitive K⁺ (K_ATP) channels and activating Ca²⁺ influx. Here, we use recombinant targeted luciferases and photon counting imaging to monitor changes in free [ATP] in subdomains of single living MIN6 and primary -cells. Resting [ATP] in the cytosol ([ATP]_c), in the mitochondrial matrix ([ATP]_m), and beneath the plasma membrane ([ATP]_pm) were similar (~1 mM). Elevations in extracellular glucose concentration (3-30 mM) increased free [ATP] in each domain with distinct kinetics. Thus, sustained increases in [ATP]_m and [ATP]_pm were observed, but only a transient increase in [ATP]_c. However, detectable increases in [ATP]_c and [ATP]_pm, but not [ATP]_m, required extracellular Ca²⁺. Enhancement of glucose-induced Ca²⁺ influx with high [K⁺] had little effect on the apparent [ATP]_c and [ATP]_m increases but augmented the [ATP]_pm increase. Underlying these changes, glucose increased the mitochondrial proton motive force, an effect mimicked by high [K⁺]. These data support a model in which glucose increases [ATP]_m both through enhanced substrate supply and by progressive Ca²⁺-dependent activation of mitochondrial enzymes. This may then lead to a privileged elevation of [ATP]_pm, which may be essential for the sustained closure of K_ATP channels. Luciferase imaging would appear to be a useful new tool for dynamic in vivo imaging of free ATP concentration.

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