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Control of mitochondrial motility and distribution by the calcium signal

Muqing Yi, David Weaver, and György Hajnóczky

Department of Pathology, Anatomy, and Cell Biology, Thomas Jefferson University, Philadelphia, PA 19107

Correspondence to Gyorgy Hajnóczky: gyorgy.hajnoczky{at}jefferson.edu

Mitochondria are dynamic organelles in cells. The control of mitochondrial motility by signaling mechanisms and the significance of rapid changes in motility remains elusive. In cardiac myoblasts, mitochondria were observed close to the microtubular array and displayed both short- and long-range movements along microtubules. By clamping cytoplasmic [Ca²⁺] ([Ca²⁺]_c) at various levels, mitochondrial motility was found to be regulated by Ca²⁺ in the physiological range. Maximal movement was obtained at resting [Ca²⁺]_c with complete arrest at 1–2 µM. Movement was fully recovered by returning to resting [Ca²⁺]_c, and inhibition could be repeated with no apparent desensitization. The inositol 1,4,5-trisphosphate– or ryanodine receptor-mediated [Ca²⁺]_c signal also induced a decrease in mitochondrial motility. This decrease followed the spatial and temporal pattern of the [Ca²⁺]_c signal. Diminished mitochondrial motility in the region of the [Ca²⁺]_c rise promotes recruitment of mitochondria to enhance local Ca²⁺ buffering and energy supply. This mechanism may provide a novel homeostatic circuit in calcium signaling.

Abbreviations used in this paper: _m, mitochondrial membrane potential; Caff, caffeine; ECM, extracellular medium; Iono, Ionomycin; IP₃, inositol 1,4,5-trisphosphate; MF, microfilament, mitoYFP, enhanced-YFP targeted to the mitochondrial matrix; MT, microtubule, RyR, ryanodine receptor; Tg, thapsigargin; VP, vasopressin.

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