Advances in research on the prenatal development of skeletal muscle in animals in relation to the quality of muscle-based food. I. Regulation of myogenesis and environmental impact

Abstract

Skeletal muscle development in vertebrates – also termed myogenesis – is a highly integrated process. Evidence to date indicates that the processes are very similar across mammals, poultry and fish, although the timings of the various steps differ considerably. Myogenesis is regulated by the myogenic regulatory factors and consists of two to three distinct phases when different fibre populations appear. The critical times when myogenesis is prone to hormonal or environmental influences depend largely on the developmental stage. One of the main mechanisms for both genetic and environmental effects on muscle fibre development is via the direct action of the growth hormone–insulin-like growth factor (GH–IGF) axis. In mammals and poultry, postnatal growth and function of muscles relate mainly to the hypertrophy of the fibres formed during myogenesis and to their fibre-type composition in terms of metabolic and contractile properties, whereas in fish hyperplasia still plays a major role. Candidate genes that are important in skeletal muscle development, for instance, encode for IGFs and IGF-binding proteins, myosin heavy chain isoforms, troponin T, myosin light chain and others have been identified. In mammals, nutritional supply in utero affects myogenesis and the GH–IGF axis may have an indirect action through the partitioning of nutrients towards the gravid uterus. Impaired myogenesis resulting in low skeletal myofibre numbers is considered one of the main reasons for negative long-term consequences of intrauterine growth retardation. Severe undernutrition in utero due to natural variation in litter or twin-bearing species or insufficient maternal nutrient supply may impair myogenesis and adversely affect carcass quality later in terms of reduced lean and increased fat deposition in the progeny. On the other hand, increases in maternal feed intake above standard requirement seem to have no beneficial effects on the growth of the progeny with myogenesis not or only slightly affected. Initial studies on low and high maternal protein feeding are published. Although there are only a few studies, first results also reveal an influence of nutrition on skeletal muscle development in fish and poultry. Finally, environmental temperature has been identified as a critical factor for growth and development of skeletal muscle in both fish and poultry.

Epigenetics and developmental programming of welfare and production traits in farm animals

“…There are numerous reviews (e.g. Brameld and Daniel 2008;Rehfeldt et al 2011b) describing this process and the factors that regulate it, including cross-species comparisons (Rehfeldt et al 2011a), and only a brief summary is provided here.…”

“…double muscling in cattle) or environmental (e.g. maternal nutrition or administration of hormones) factors, but only if the environmental insults take place at specific times during gestation (see Brameld and Daniel 2008;Rehfeldt et al 2011aRehfeldt et al , 2011b. Tables S4 and S5 summarise studies investigating the effects of maternal nutrition on muscle fibre formation in sheep and pigs.…”

Skeletal muscle development in vertebrate animals

“…Further differentiation of dermomyotome creates dorsal-lateral dermatome and myotome which give rise to dermis and axial musculature, respectively (Bumcrot and McMahon, 1995). The review of Rehfeldt et al, (2011a) stated that the first phase of skeletal trunk muscle formation in mammals, poultry and fish is primary myotome which originates from the four epithelial borders of the dermomyotome. In addition, the central region of that part changes epithelial to mesenchymal transition in the second phase to release paired box (PAX) 3/7-positive cells into primary myotome and these cells evolve into embryonic myoblasts or fetal myoblasts or satellite cells.…”

“…The timing of different developmental stages varied significantly but the end products are same to form multinucleated myofibers with contractile capability (Knight and Kothary, 2011). Myogenesis is controlled by an elaborate interplay of extrinsic and intrinsic regulatory mechanisms (Bentzinger et al, 2012) regulated by myogenic regulatory factors including 2-3 distinct phases, in addition, protein kinase family which transmits and executes signals originated by promyogenic stimuli (Rehfeldt et al, 2011a andKnight andKothary, 2011). The key factors of muscle growth are proliferation and differentiation of myogenic cells (prenatal stage) ( Figure 2) and satellite cells (postnatal stage) (Figure 3).…”

“…The growth and myogenic regulatory factors are associated with skeletal muscle growth through cell proliferation and differentiation (Parakati and DiMario, 2013) in numerous tissues of animals. Growth rate and growth potential are undoubtedly heritable characteristics and also relate to their fiber-type composition, particularly in terms of contractile speed and metabolism, but different environmental factors like ambient temperature and food availability could also affect the growth of all species (Leatherland, 1994 andRehfeldt et al, 2011a). Skeletal muscle could regenerate and restore the cellular architecture completely Garry, 2006 andMeadows et al, 2008) in response to repeated injuries by one type muscle stem cell called satellite cells.…”