A Way in Which Mitochondrial DNA Becomes Misplaced, Provoking Inflammation

Cells respond to the presence of DNA in the cytoplasm with inflammatory signaling, an evolved innate immune response that serves to protect against viral and bacterial infection. This becomes a problem when mitochondria become dysfunctional, as mitochondria contain their own small genome, the mitochondrial DNA. In the context of age-related mitochondrial dysfunction, and a number of other circumstances, fragments of mitochondrial DNA can find their way into the cell cytoplasm. The result is a link between mitochondrial dysfunction and the chronic inflammation of aging, though it remains unclear as to how much of this characteristic unresolved inflammatory signaling is the result of mislocated DNA versus, say, the presence of senescent cells, or other contributions. Is there something that can be done to block this unwanted inflammatory signaling, short of repairing or replacing dysfunctional mitochondria throughout the body? Perhaps, perhaps not, but further research is the only way to find out.

Mitochondrial DNA (mtDNA) encodes essential subunits of the oxidative phosphorylation system, but is also a major damage-associated molecular pattern (DAMP) that engages innate immune sensors when released into the cytoplasm, outside of cells or into circulation. As a DAMP, mtDNA not only contributes to anti-viral resistance, but also causes pathogenic inflammation in many disease contexts. Cells experiencing mtDNA stress caused by depletion of the mtDNA-packaging protein, mitochondrial transcription factor A (TFAM) or during herpes simplex virus-1 infection exhibit elongated mitochondria, enlargement of nucleoids (mtDNA-protein complexes) and activation of cGAS-STING innate immune signalling via mtDNA released into the cytoplasm. However, the relationship among aberrant mitochondria and nucleoid dynamics, mtDNA release, and cGAS-STING activation remains unclear.

Here we show that, under a variety of mtDNA replication stress conditions and during herpes simplex virus-1 infection, enlarged nucleoids that remain bound to TFAM exit mitochondria. Enlarged nucleoids arise from mtDNA experiencing replication stress, which causes nucleoid clustering via a block in mitochondrial fission at a stage when endoplasmic reticulum actin polymerization would normally commence, defining a fission checkpoint that ensures mtDNA has completed replication and is competent for segregation into daughter mitochondria. Chronic engagement of this checkpoint results in enlarged nucleoids trafficking into early and then late endosomes for disposal. Endosomal rupture during transit through this endosomal pathway ultimately causes mtDNA-mediated cGAS-STING activation. Thus, we propose that replication-incompetent nucleoids are selectively eliminated by an adaptive mitochondria-endosomal quality control pathway that is prone to innate immune system activation, which might represent a therapeutic target to prevent mtDNA-mediated inflammation during viral infection and other pathogenic states.

Link: https://doi.org/10.1038/s41556-023-01343-1

Comments

Over time (say as we age) Mitochondria could evolve enough to begin the genetically diverge enough to begin to fight each other.
Could this account for a lot of aging?

Posted by: Rob at March 9th, 2024 10:18 AM
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