Skeletal muscle reprogramming enhances reinnervation after peripheral nerve injury
Peripheral Nerve Injuries (PNI) affect more than 20 million Americans and severely impact quality of life by causing long-term disability. PNI is characterized by nerve degeneration distal to the site of nerve injury resulting in long periods of skeletal muscle denervation. During this period, muscle fibers atrophy and frequently become incapable of "accepting" innervation because of the slow speed of axon regeneration post injury. We hypothesize that reprogramming the skeletal muscle to an embryonic-like state may preserve its reinnervation capability following PNI. To this end, we generate a mouse model in which NANOG, a pluripotency-associated transcription factor is expressed locally upon delivery of doxycycline (Dox) in a polymeric vehicle. NANOG expression in the muscle upregulates the percentage of Pax7+ nuclei and expression of eMYHC along with other genes that are involved in muscle development. In a sciatic nerve transection model, NANOG expression leads to upregulation of key genes associated with myogenesis, neurogenesis and neuromuscular junction (NMJ) formation. Further, NANOG mice demonstrate extensive overlap between synaptic vesicles and NMJ acetylcholine receptors (AChRs) indicating restored innervation. Indeed, NANOG mice show greater improvement in motor function as compared to wild-type (WT) animals, as evidenced by improved toe-spread reflex, EMG responses and isometric force production. In conclusion, we demonstrate that reprogramming muscle can be an effective strategy to improve reinnervation and functional outcomes after PNI.
Authors
- Gabriella Kayal
- Stelios T. Andreadis (ORCID: https://orcid.org/0000-0001-9885-0457)
- Nika Rajabian (ORCID: https://orcid.org/0000-0002-9963-4024)
- Reilly Ellis
- James Jablonski
- Susan B. Udin (ORCID: https://orcid.org/0000-0001-5542-6314)
- John Toftegaard
- Kirkwood E. Personius (ORCID: https://orcid.org/0000-0001-6391-2953)
- Shahryar Shahini (ORCID: https://orcid.org/0000-0003-3813-6424)
- Kelly Cristine Santos Roballo (ORCID: https://orcid.org/0000-0001-8420-9159)
- Pihu Mehrotra (ORCID: https://orcid.org/0000-0001-9369-5013)
- Carey W. Hung
- Song Liu (ORCID: https://orcid.org/0000-0001-6351-2941)
- Jianmin Wang (ORCID: https://orcid.org/0000-0001-7527-0409)
- Yali Zhang (ORCID: https://orcid.org/0000-0002-8328-0591)
Institutions
- Roswell Park Comprehensive Cancer Center (US)
- Virginia–Maryland College of Veterinary Medicine (US)
- Buffalo BioLabs (US)
- University at Buffalo, State University of New York (US)
- Center for Excellence in Education (US)
- Edward Via College of Osteopathic Medicine (US)
Publication Details
- Journal
- Nature Communications
- Published
- 2024-10-25
- DOI
- https://doi.org/10.1038/s41467-024-53276-4
- Citations
- 21
- Primary Topic
- Nerve injury and regeneration
- Type
- article
- Field-Weighted Citation Impact
- 5.63
Funders
- Foundation for the National Institutes of Health
- State University of New York
- National Institutes of Health