SARS-CoV-2 infected patients suffer from a spectrum of symptoms, yet the molecular mechanisms responsible for these have yet to be elucidated. One of these symptoms involves musculoskeletal myopathies. At the body level, these are characterized as muscle fatigue, weakness, pain, and lower exercise capacity. Whereas at the tissue level, there is evidence of skeletal muscle atrophy, necrosis, and fiber regeneration. Furthermore, at the cellular level, issues with metabolism and mitochondrial function have been shown. Interestingly proper mitochondrial biogenesis and protein function are crucial for skeletal muscle development and are dependent on copper (Cu) availability. Our lab has shown that disruption of the Cu regulatory network results in disruption of mitochondrial protein function, and overall skeletal muscle proliferation and differentiation. SARS-CoV-2 encodes a gene known as ORF3A, a proposed viroporin or ion channel, which we propose acts as a potential metal-transporter. Structural and sequence homology analyses identified several residues which may coordinate transition metals and located in key positions similarly to Cu+-ATPases and zinc (Zn2+)-transporters. We hypothesized that when ORF3A is expressed in human cells, it may transport metal ions, which may affect metal homeostasis and mitochondrial function in tissues, including skeletal muscle. To test this hypothesis, we characterized ORF3A using biochemical and cell biology methods. We cloned, and purified recombinant ORF3A and showed that it can bind Cu in a one-to-one ratio. Exogeneous ORF3A, transformed into an Escherichia coli strain lacking the CopA Cu exporter and susceptible to metal toxicity, rescues this phenotype. Transient expression of ORF3A in the established cultured skeletal muscle cell line C2C12 induced apoptosis. ORF3A was located in the cytoplasm with heavy concentration in the perinuclear region, partially localizing in the Golgi apparatus. Importantly, ORF3A altered the expression of several cuproproteins including mtf1 and atp7a. Cell blebbing was also observed where the Cu+-chaperone atox1 was located at these structures. Mitochondria of ORF3A expressing cells had an increase in reactive oxygen species and a disruption of membrane potential in this organelle. These features suggested a significant alteration of Cu homeostasis which resulted in mitochondrial dysfunction. In addition, we detected an increase in lysosome numbers containing elevated levels of Zn. Our work has the potential to provide a novel mechanism by which metal homeostasis and mitochondrial function is altered, a process which may be related to the muscular phenotype observed in long-Covid patients.
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