Abstract
Extraocular muscles (EOMs) show resistance to muscle dystrophies and sarcopenia. It has been recently demonstrated that they are endowed with different types of myogenic cells, all of which present an outstanding regenerative potential. Neurotrophins are important modulators of myogenic regeneration and act promoting myoblast proliferation, enhancing myogenic fusion rates and protecting myotubes from inflammatory stimuli. Here, we adapted the pre-plate cell isolation technique to obtain myogenic progenitors from the rat EOMs, and quantified their in vitro expression of neurotrophins and their receptors by RT–qPCR and immunohistochemistry, respectively. The results were compared with the expression on progenitors isolated from buccinator, tongue and limb muscles. Our quantitative analysis of brain-derived neurotrophic factor (BDNF), nerve growth factor (NGF) and neurotrophin-3 (NT-3) transcripts showed, for the first time, that EOMs-derived cells express more of these factors and that they expressed TrkA, but not TrkB and TrkC receptors. On the contrary, the immunofluorescence analysis demonstrated high expression of p75NTR on all myogenic progenitors, with the EOMs-derived cells showing higher expression. Taken together, these results suggest that the intrinsic trophic differences between EOMs-derived myogenic progenitors and their counterparts from other muscles could explain why those cells show higher proliferative and fusion rates, as well as better regenerative properties.
Highlights
Extraocular muscles (EOMs) are a group of craniofacial skeletal muscles that are responsible for eye movements
We found no differences between the weight of the extensor digitorum longus (EDL) and tongue muscles, the EOM weighted less than half the value of the former muscles (one-way ANOVA test: F(3,17 ) = 122.578, P < 0.001, Holm–Sidak method for post-hoc comparison, P < 0.05)
We aimed to investigate if there were intrinsic trophic differences between muscle progenitors derived from the EOMs, the muscles of the tongue, the buccinator and the EDL, that could explain why the EOMs satellite cells (SCs) show higher proliferative and fusion rates, features that seem to be responsible for the extraordinary EOMs regenerative properties and their resistance to certain diseases [11,13]
Summary
Extraocular muscles (EOMs) are a group of craniofacial skeletal muscles that are responsible for eye movements. Specialized, they are fundamentally distinct from other muscles and have been classified as a separate muscle allotype [1]. EOMs differ from other cranial, limb and body muscles developmentally, anatomically, structurally, biochemically and physiologically [2,3,4,5] They even respond differently to aging [6] and to certain disorders affecting the skeletal muscle, remaining anatomically and functionally intact even at the late stages of Duchenne muscular dystrophy (DMD) in humans [7] and in animal models of this disorder [8]. In recent years, the discovery of the unique properties of EOM myogenic progenitors and their proliferative and regenerative features [11,12,13] point them as fundamental factors contributing to the normal EOM structure and function in DMD and other muscle disorders
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