Differential muscle regulatory factor gene expression between larval and adult myogenesis in the frog Xenopus laevis: adult myogenic cell-specific myf5 upregulation and its relation to the notochord suppression of adult muscle differentiation

Abstract

During Xenopus laevis metamorphosis, larval-to-adult muscle conversion depends on the differential responses of adult and larval myogenic cells to thyroid hormone. Essential differences in cell growth, differentiation, and hormone-dependent life-or-death fate have been reported between cultured larval (tail) and adult (hindlimb) myogenic cells. A previous study revealed that tail notochord cells suppress terminal differentiation in adult (but not larval) myogenic cells. However, little is known about the differences in expression patterns of myogenic regulatory factors (MRF) and the satellite cell marker Pax7 between adult and larval myogenic cells. In the present study, we compared mRNA expression of these factors between the two types. At first, reverse transcription polymerase chain reaction analysis of hindlimb buds showed sequential upregulation of myf5, myogenin, myod, and mrf4 during stages 50-54, when limb buds elongate and muscles begin to form. By contrast, in the tail, there was no such increase during the same period. Secondary, these results were duplicated in vitro: adult myogenic cells upregulated myf5, myod, and pax7 in the early culture period, followed by myogenin upregulation and myotube differentiation, while larval myogenic cells did not upregulate these genes and precociously started myotube differentiation. Thirdly, myf5 upregulation and early-phase proliferation in adult myogenic cells were potently inhibited by the presence of notochord cells, suggesting that notochord cells suppress adult myogenesis through inhibiting the transition from Myf5(-) stem cells to Myf5(+) committed myoblasts. All of the data presented here suggest that myf5 upregulation can be a good criterion for the activation of adult myogenesis during X. laevis metamorphosis.

Development of skeletal muscle and expression of myogenic regulatory factors during embryonic development in Jinding ducks (Anas platyrhynchos domestica)

“…Many genes related to muscle formation, such as MRF, are active during this period (Cao et al, 2006;Hennebry et al, 2009;Yamane and Nishikawa, 2013). In the present study, the MyoD gene expression patterns differed between BM and LM, with lower expression levels in BM from embryonic d 13 to 21 compared with LM, whereas the opposite pattern was found from embryonic d 25 to 27.…”

Evolutionary history and epigenetic regulation of the three paralogous pax7 genes in rainbow trout

“…Using such an in vitro model for experimentation, Neil Bower and Ian Johnston (Bower and Johnston 2010) documented that pax7 expression is up regulated during the differentiation of MSCs from Atlantic salmon ( Salmo salar ). Pax7 , the canonical marker of MSCs in birds and mammals (Seale et al 2000, Halevy et al 2004), is rapidly down-regulated upon induction of MSC differentiation in rodents, birds, and Xenopus (Halevy et al 2004, Zammit et al 2004, Yamane and Nishikawa 2013), in agreement with its function in survival and quiescence of MSCs. Thus, the continued pax7 transcript expression in salmonid fishes is highly unusual in light of the current literature and warrants further investigation.…”

Making muscle: Morphogenetic movements and molecular mechanisms of myogenesis in Xenopus laevis

“…This is supported by experiments in mice suggesting that Myf5 and MyoD regulate independent myogenic compartments [107]. In fact, the successive myogenic waves during X. laevis somitogenesis include myf5 -dependent and independent myogenic waves, further supporting the unique contributions of myf5 during larval [31] and adult [108] myogenesis. As mentioned above, both MyoD and Myf5 are typically associated with the specification stage of myogenesis and have many overlapping, but also distinct functions.…”