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https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4440565/#!po=0.409836

Features of brain energy metabolism

In the human body, the brain has the greatest demand for oxygen and is susceptible to disturbances in energy metabolism, which is determined by its high metabolic rate, high oxygen consumption and low energy reserves. Mitochondria are the key sites of oxidative phosphorylation (OXPHOS) and the synthesis of adenosine triphosphate (ATP). The redox enzymes and the coenzymes involved in the respiratory chain lie in the mitochondrial inner membrane in close proximity. Electrons passing through the respiratory chain drive protons from the matrix side to the cytoplasmic side across the mitochondrial inner membrane. When protons reflux along the concentration gradient, the energy released is used by ATP synthase to catalyze ATP synthesis.

In addition to energy conversion, mitochondria also play other important roles, such as in the regulation of apoptosis and Ca2+ storage. Mitochondria are not only the starting point of many signal transduction pathways but also the target.

Effects of MW radiation on mitochondrial energy metabolism

MW radiation is detrimental to brain energy metabolism. Intrinsically, neurons are extremely sensitive to a reduced ATP availability. As the main source of energy, mitochondria are prone to MW radiation-induced injury. Wang et al. [26] exposed monkeys to MW radiation with average power densities of 5 mW/cm2 and 11 mW/cm2 for 10 s and 4.68 μW/cm2 for 12 h/d for 30 d cumulatively. Abnormalities in mitochondrial function-related metabolites in urine, such as succinic acid, citric acid and 2-keto-glutaric acid, were induced after a single radiation event of 5 mW/cm2 and 11 mW/cm2 and after a long-term radiation of 4.68 μW/cm2, revealing by metabolomics the hypersensitivity of mitochondria to MW radiation.

Effects of MW radiation on mitochondrial structure

MW radiation leads to mitochondrial structural damage, primarily observed as mitochondrial swelling and cavitation and disorganized, broken and sparse cristae.

To some extent, MW radiation affects mitochondria structurally in a dose-dependent manner. Zhao et al. [5] exposed male Wistar rats to MW radiation with average power densities of 2.5, 5 and 10 mW/cm2, with the specific absorption rates (SAR) of 1.05, 2.1 and 4.2 W/kg, respectively, for 6 min/d for 30 d. In the hippocampus of the MW-exposed rats, the mitochondria were swollen and vacuolized, and the cristae were disordered and fewer in number. In addition, these ultrastructural changes in the mitochondria tended to be more severe relative to the increasing SAR. Xie et al. [27] exposed male Wistar rats to MW radiation for 1 h at average power densities of 3 and 30 mW/cm2, respectively. No significant changes occurred in the mitochondria of the hippocampus or cerebral cortex in the 3 mW/cm2 group, while the mitochondria in the 30 mW/cm2 group did become damaged. These results suggest that, within a certain range, the degree of mitochondrial structural damage positively correlates with the dose of MW radiation.

MW radiation damaging mitochondrial structures obeys a time-response relationship. Xie et al. [27] exposed male Wistar rats to MW radiation (30 mW/cm2, duration: 1 h). Immediately after radiation, the mitochondrial ultrastructure showed a slight disturbance in the rat hippocampus and cerebral cortex; 3 h after radiation, the visible swelling of the mitochondria increased significantly and cristae became disorganized, broken and sparse; 24 h after radiation, mitochondrial degeneration was observed, demonstrated by myelin-like structures and occasional dense deposits in the mitochondria. In short, ultrastructural changes in the rat brain mitochondria were induced within 24 h of the post-30 mW/cm2 MW radiation exposure.

Long-term and low-dose cumulative MW radiation leads to significant damage in mitochondria. Dong et al. [21] exposed SD rats to MW radiation (4.68 μW/cm2, 12 h/d, duration: 30 d), which resulted in similar structural changes, such as swelling and cavitation in the mitochondria of the radiation-exposed rat hippocampus and cerebral cortex.

Effects of MW radiation on mitochondrial energy metabolism

Reduced ATP content

As the “cell power plant”, the most important function of mitochondria is to provide energy for the cell; therefore, intracellular ATP content is one of the most direct and objective indicators in the evaluation of mitochondrial function. In addition, ATPases hydrolyze ATP to ADP and release the energy stored in ATP.

Certain doses of MW radiation cause reduction in mitochondrial ATP synthesis. Zhao et al. [25] exposed male Wistar rats to pulsed MW radiation (30 mW/cm2, duration: 5 min). The results showed that the content of mitochondrial ATP in the hippocampus of MW-exposed rats dropped to the lowest levels 3 d after radiation and recovered 7 d after radiation, while the activity of the ATPases was greatly enhanced 3 d after radiation and recovered 7 d after radiation, suggesting a compensatory role played by this negative feedback regulation. Sander et al. [28] exposed SD rats to MW radiation with a frequency of 591 MHz at an average power density of 13.8 mW/cm2, which induced a reduced availability of ATP, resulting in brain energy metabolism disorders.

Decreased succinate dehydrogenase (SDH) activity

As one of the key enzymes of mitochondrial energy metabolism, SDH binds to the mitochondrial inner membrane and catalyzes the dehydrogenation of succinate to generate ATP ultimately, forming a bridge between the Krebs cycle and OXPHOS.

MW radiation reduces the activity of SDH. Zhao et al. [25] exposed male Wistar rats to pulsed MW radiation (30 mW/cm2, duration: 5 min). The SDH activity of the MW-exposed rat hippocampus decreased significantly 6 h after radiation, resulting in abnormalities in mitochondrial energy metabolism. Wang et al. [29] exposed Wistar rats to high power microwave (HPM) radiation of 10, 30 and 100 mW/cm2for 5 min, respectively. They also found reduced SDH activity present in every exposure group, which recovered 7 d after radiation. Another study exposed male Wistar rats to MW radiation of 30 mW/cm2for 15 min. The SDH activity of the MW-exposed rat hippocampus did not change significantly at 14 d after radiation, indicating that the MW radiation-induced decline in SDH activity is reversible under certain conditions [23].

Suppressed cytochrome c oxidase (COX) activity

COX is embedded in the mitochondrial inner membrane and is the terminal complex of the mitochondrial electron transport chain. As another one of the key enzymes of mitochondrial energy metabolism, COX is the only enzyme to transport electrons to oxygen to produce H2O and ATP [30,31]. It is believed that 90% of intracellular molecular oxygen is utilized by COX [32].

Certain doses of MW radiation negatively impact the activity of COX. Wang et al. [33] exposed primary cultures of cerebral cortical neurons of Wistar rats to continuous MW radiation of 900 MHz, with SARs of 0.38, 0.76, 1.15, 2.23 and 3.22 W/kg, respectively, for 2 h/d for 4 to 6 d. The results showed that the toxic effects of MW radiation on COX activity accumulated and that there was a dose-dependent relationship. Xiong et al. [34] used MW radiation of 30 mW/cm2 to irradiate male Wistar rats. The decreased COX activity and the reduced expression of COX I/IV mRNA and COX I protein were found after MW radiation, illustrating that MW radiation impacted COX activity at multiple levels.

Potential mechanisms involved in MW radiation-induced disturbances in mitochondrial energy metabolism

By the rapid development of modern molecular biology techniques, studies on the mechanisms of the biological effects of MW radiation have been possible at the cellular and molecular levels. This section will review the potential mechanisms of MW radiation-induced brain energy metabolism disorders from seven aspects, including gene expression, the mitochondrial membrane, apoptosis, oxidative stress (OS), Ca2+ overload, mitochondrial DNA and the involved signal transduction pathways.

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