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J Biol Chem, Vol. 274, Issue 14, 9305-9311, April 2, 1999

Calcium-dependent Regulation of Cytochrome c Gene Expression in Skeletal Muscle Cells
IDENTIFICATION OF A PROTEIN KINASE C-DEPENDENT PATHWAY

From the Departments of Biology and Kinesiology and Health Science, York University, Toronto, Ontario M3J 1P3, Canada

Mitochondrial biogenesis can occur rapidly in mammalian skeletal muscle subjected to a variety of physiological conditions. However, the intracellular signal(s) involved in regulating this process remain unknown. Using nuclearly encoded cytochrome c, we show that its expression in muscle cells is increased by changes in cytosolic Ca²⁺ using the ionophore A23187. Treatment of myotubes with A23187 increased cytochrome c mRNA expression up to 1.7-fold. Transfection experiments using promoter-chloramphenicol acetyltransferase constructs revealed that this increase could be transcriptionally mediated since A23187 increased chloramphenicol acetyltransferase activity by 2.5-fold. This increase was not changed by KN62, an inhibitor of Ca²⁺/calmodulin-dependent kinases II and IV, and it was not modified by overexpression of protein kinase A and cAMP response element-binding protein, demonstrating that the A23187 effect was not mediated through Ca²⁺/calmodulin-dependent kinase- or protein kinase A-dependent pathways. However, treatment of myotubes with staurosporine or 12-O-tetradecanoylphorbol-13-acetate reduced the effect of A23187 on cytochrome c transactivation by 40-50%. Coexpression of the Ca²⁺-sensitive protein kinase C isoforms  and _II, but not the Ca²⁺-insensitive  isoform, exaggerated the A23187-mediated response. The short-term effect of A23187 was mediated in part by mitogen-activated protein kinase (extracellular signal-regulated kinases 1 and 2) since its activation peaked 2 h after A23187 treatment, and cytochrome c transactivation was reduced by PD98089, a mitogen-activated protein kinase/extracellular signal-regulated kinase kinase inhibitor. These results demonstrate the existence of a Ca²⁺-sensitive, protein kinase C-dependent pathway involved in cytochrome c expression and implicate Ca²⁺ as a signal in the up-regulation of nuclear genes encoding mitochondrial proteins.

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