Low Magnetic Fields Stimulate Cardiac Mitochondrial Bioenergetics with a Bell-Shaped Response: Possibly Via a Radical Pair Mechanism

Studies have shown that low magnetic fields (LMFs) of less than 1 x 10-3 Tesla (T) affect numerous biological events, including bacteria and plant growth, bird migration, and human brain activity. On a cellular level, LMFs affect ion channel activities, intracellular Ca2+ concentrations, and mitochondrial reactive oxygen species (mROS) generation. However, the mechanisms that could account for these effects are controversial. Here, we show that applying a static LMF, ranging from [~]2.7 x 10-4 to [~]1.9 x 10-3 T, to mitochondria isolated from adult rat hearts produced a bell-shaped increase in maximal respiration (Vmax) up to 40%. A similar LMF-induced increase in Vmax was also observed in mitochondria isolated from rat hearts subjected to ischemia-reperfusion (I-R) injury. We then obtained data showing that LMF- mediated bell-shaped response was also observed in the activity of several enzymes involved in oxidative phosphorylation (OXPHOS), including Complexes II, III, and V, and citrate synthase. By contrast, similar LMF caused little change in the enzymatic activity of Complex I. Interestingly, mROS generation responded to LMF with an inverted bell-shaped decrease. We propose a radical pair mechanism of magnetoreception in cytochromes, catalytical reactions, and iron-sulfur clusters within the OXPHOS enzymes to explain how an LMF can increase the likelihood of electron spin transitions from singlet to triplet state and reverse it as the magnetic field strength further increases, resulting in a bell-shaped response. Our results indicate that a narrow range of LMF can enhance mitochondrial bioenergetics and decrease mROS. This may provide a non-invasive approach to treating diseases, such as I-R injury, when energy generation is compromised and oxidative stress is magnified.