Distinct Embryonic Origin and Injury Response of Resident Stem Cells in Craniofacial Muscles

Abstract

Craniofacial muscles emerge as a developmental novelty during the evolution from invertebrates to vertebrates, facilitating diversified modes of predation, feeding and communication. In contrast to the well-studied limb muscles, knowledge about craniofacial muscle stem cell biology has only recently starts to be gathered. Craniofacial muscles are distinct from their counterparts in other regions in terms of both their embryonic origin and their injury response. Compared with somite-derived limb muscles, pharyngeal arch-derived craniofacial muscles demonstrate delayed myofiber reconstitution and prolonged fibrosis during repair. The regeneration of muscle is orchestrated by a blended source of stem/progenitor cells, including myogenic muscle satellite cells (MuSCs), mesenchymal fibro-adipogenic progenitors (FAPs) and other interstitial progenitors. Limb muscles host MuSCs of the Pax3 lineage, and FAPs from the mesoderm, while craniofacial muscles have MuSCs of the Mesp1 lineage and FAPs from the ectoderm-derived neural crest. Both in vivo and in vitro data revealed distinct patterns of proliferation and differentiation in these craniofacial muscle stem/progenitor cells. Additionally, the proportion of cells of different embryonic origins changes throughout postnatal development in the craniofacial muscles, creating a more dynamic niche environment than in other muscles. In-depth comparative studies of the stem cell biology of craniofacial and limb muscles might inspire the development of novel therapeutics to improve the management of myopathic diseases. Based on the most up-to-date literature, we delineated the pivotal cell populations regulating craniofacial muscle repair and identified clues that might elucidate the distinct embryonic origin and injury response in craniofacial muscle cells.

Fibroadipogenic Progenitors Regulate the Basal Proliferation of Satellite Cells and Homeostasis of Pharyngeal Muscles via HGF Secretion

“…Neural crest-derived muscle connective tissues, precursors of FAPs, are required for craniofacial muscle development and morphogenesis ( Noden and Trainor, 2005 ; Rinon et al, 2007 ). Although less well studied, FAPs were thought to have a profound role in craniofacial muscle homeostasis and regeneration ( Cheng et al, 2021 ). Interestingly, HGF is one of the critical factors that induce migration of muscle progenitor cells that express cMET as an HGF receptor for muscle development ( Bladt et al, 1995 ; Dietrich et al, 1999 ).…”

New Perspectives for Postmortem Human Satellite Cells of Different Embryological Origin

“…Postmortem thyrohyoid hMPCs showed peculiar spontaneous [Ca 2+ ] waves lasting tens of minutes. It is worth mentioning that embryological pharyngeal arches originate in not only neck muscles but also cardiomyocytes, which have been demonstrated to be able to give the oscillatory pattern of resting cytosolic calcium ( Eisner et al, 2017 ; Cheng et al, 2021 ). This creates proactive behavior of the presomite hMPCs, a sort of pacemaking prone to contraction.…”

“…However, to our knowledge, the data we reported in this study are the first demonstration that pre-somitic SCs can be achieved from postmortem presomite muscles, established in culture, and used for studies on muscle regeneration despite the fact that craniofacial muscle regeneration has physiological peculiar properties and promising characteristics observed during aging or muscle disease. Interestingly, eye extrinsic muscles do not show signs of sarcopenia and are less affected by muscular dystrophies ( McLoon et al, 2007 ; La Rovere et al, 2014 ; Cheng et al, 2021 ). The amount of SCs we obtained by thyrohyoid is also impressive: if we consider that 1 mg of muscle furnished about 5 × 10 3 cells at the first PDL, we had 1 g of muscle.…”

“…However, scarce data exist on postmortem SCs and any of their functional features. Not to mention the craniofacial muscle stem cell biology, which only recently has started to be gathered ( Cheng et al, 2021 ). Indeed, most data of these muscles remain at the level of tissue description, few indications about their SCs, and no data exist at the postmortem level for presomite SC features.…”

Physiology of the tongue with emphasis on taste transduction

“…Unlike other muscles in the body, the cellular and molecular responses of craniofacial muscles have not been extensively studied ( 204 ). Muscle regeneration is mainly orchestrated by a population of muscle stem cells, termed satellite cells (MuSCs).…”