Investigators at University of British Columbia have reported the precise cellular populations responsible for the inability to regenerate muscle tissues in muscular dystrophy.
The team also showed that by depleting the macrophages that were preventing regeneration, they could affect the composition of muscle fibers towards so-called slow twitch fibers, which are more damage-resistant than their fast-twitch counterparts.
They reported their findings in the June 29, 2022, issue of Science Translational Medicine.
Muscle regeneration is rather unique, as muscle tissue is one the few tissues that is capable of completely restoring function after acute injury.
In response to cell death after high-intensity muscle strain, macrophage-rich cell populations first clean up the dead muscle cell mess and then begin to process of regenerating new muscle tissue.
However, patients with muscular dystrophy cannot fully regenerate tissues after strain owing to mutations in the gene coding for the dystrophin protein. The cumulative damage leads to functional loss as their muscles are not capable of completely recovering and regenerating.
Principal investigator Fabio Rossi, professor of biomedical engineering and medical genetics at the University of British Columbia, told BioWorld Science that "scientifically we have finally defined the resident macrophages involved in the muscle regenerative process. We knew how to distinguish them from the incoming cells before, but we weren't sure exactly which macrophages markers would be associated with regeneration because the cells tend to look very much the same.
"From a translational point of view, depleting these subtypes of macrophages that we identified cells have an effect on switching the muscle fiber to a slower type of muscle fiber that has been known for years to be more resistant to the damage that is caused by this genetic mutation of dystrophin."
Both muscle-resident macrophage and bone marrow-derived macrophages affect muscle regeneration. In the study, the researchers used parabiosis and lineage tracing to differentiate the origins of macrophage populations that affected the muscles. Thereafter, they examined the possibility that the colony-stimulating factor 1 receptor (CSF1R) inhibition could influence these cell populations.
Using mouse models of muscular dystrophy, the researchers observed that CSF1R inhibition prevented muscle damage after strain in part by switching muscle fiber types from fast to slow.
In previous studies, researchers in Rossi's laboratory had observed that brain-resident microglia are exceptionally dependent on continual signaling from CSF1R and that after blocking CSF1R signaling, this microglia population almost disappears. Rossi decided to explore whether this is the same approach would work for similar macrophage-like cell types found in muscles. They tested CSF1R inhibition in muscles and discovered this to be true.
Treatment of muscular dystrophy mouse models with an inhibitor of CSF1R led to depletion of the macrophages that were preventing the regeneration of muscle tissue.
Turalio (pexidartinib; Daiichi Sankyo Co. Ltd.) is approved for the treatment of tenosynovial giant cell tumor, and there are multiple CSF1R inhibitors in clinical trials.
To Rossi, the most impressive observation in the study was the complete lack of muscle damage as shown by absence of detectable creatine kinase in muscular dystrophy mice that had been put on a treadmill that were treated with the CSF1R inhibitor. By contrast, untreated mice exhibited muscle damage after being put on a treadmill. Rossi emphasized that "this was a really impressive result... it's not easy to have such a dramatic change when you are working with a biological system."
The researchers plan to use larger animal models of muscular dystrophy in future experiments while also working with clinicians interested in leading clinical trials. The animal models will most likely involve rats, which are bigger than mice and exhibit more human-like pharmacology, but alternatively they may use pig or dog genetic models of muscular dystrophy.
Kinase inhibitors are notorious for their off-target effects – Turalio, for example, affects KIT and Flt3 kinases as well as CSF1R. So CSF1R inhibition as the mechanism that underlies the muscle reprogramming remains to be solidified. But Rossi pointed out that "the immediate preclinical point is that it doesn't matter how it does it. Since it works, it may potentially be exploited."