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«Arch. Tierz., Dummerstorf 48 (2005) Special Issue, 04-10 Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College Street, ...»

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Arch. Tierz., Dummerstorf 48 (2005) Special Issue, 04-10

Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College Street,

London NW1 0TU, UK

CLARE ASHTON, STEPHANIE BAYOL, GRÁINNE MCENTEE, V. MALTBY

and NEIL STICKLAND

Prenatal influences on skeletal muscle development in mammals,

birds and fish

Abstract

Muscle development can be influenced by a number of environmental factors and in a range of species.

Nutritionally disadvantaged fetuses tend to develop fewer secondary myofibres in their muscles whereas primary fibres are generally unaffected. However, prenatal nutritional restriction can lead to impaired postnatal growth without an effect on muscle fibre number. Connective tissue content in muscle is also influenced by prenatal nutrition. A 10C increase in incubation temperature in turkeys for a short period early in incubation leads to prolonged myoblast proliferation and delayed differentiation results in more muscle fibres and muscle nuclei posthatch. Lower incubation temperatures have a similar impact in fish muscle. Stimulating increased movement (through neuromuscular stimulation) in chick embryo also results in chicks at hatch with more muscle fibres and increased aerobic capacity in their muscles. Taken together, these results demonstrate that prenatal environmental factors can influence the balance between proliferation and differentiation within specific cell lineages. This in turn can affect muscle fibre number determination as well as the connective tissue and satellite cell content of muscles.

Key Words: skeletal muscle, prenatal, myogenic factors Zusammenfassung Titel der Arbeit: Pränatale Einflüsse auf die Entwicklung der Skelettmuskulatur bei Säugern, Vögeln und Fischen Bei verschiedensten Spezies lassen sich unterschiedliche Einflüsse aus der Umwelt auf die Skelettmuskelentwicklung zeigen. Unter ungünstigen Ernährungsbedingungen bilden sich bei Feten weniger sekundäre Muskelfasern aus, während die Entwicklung primärer Fasern nicht beeinflusst wird. Pränatale Futterrestriktion kann zu verminderter postnataler Wachstumsleistung führen ohne dass ein Effekt auf die Muskelfaseranzahl nachzuweisen ist. Auch das Bindegewebe der Muskulatur wird durch die pränatale Ernährung beeinflusst. Eine kurzzeitige Erhöhung der Temperatur um 1 °C während der frühen Brutphase führt bei Puten zu einer verlängerten Proliferation und verzögerten Differenzierung der Myoblasten und so zu einer erhöhten Anzahl an Muskelfasern und Muskelzellkernen nach dem Schlupf. Bei Fischen hat die Senkung der Temperatur vor dem Schlupf einen ähnlichen Effekt. Stimulation der Muskelkontraktion (durch neuromuskuläre Stimulation) bei Hühnerembryonen führt zu einer erhöhten Anzahl an Muskelfasern und erhöhter aerober Kapazität der Muskulatur beim Schlupf.

Diese Ergebnisse belegen, dass pränatal einwirkende Umweltfaktoren auf die Balance zwischen Proliferation und Differenzierung bei bestimmten Zelllinien wirken. Dies beeinflusst die Determination der Anzahl an Muskelfasern, die Ausbildung des Bindegewebes und die Bildung von Satellitenzellen im Skelettmuskel.

Schlüsselwörter: Skelettmuskel, pränatal, myogene Faktoren

Introduction Skeletal muscle develops in a biphasic manner. During embryonic development, myoblasts proliferate and then line up and fuse to form a population of large primary myofibres. A larger population of smaller secondary myofibres then form on their surfaces (REHFELDT et al., 1999). As opposed to birds and mammals, whose myofibre number is fixed at birth (in most species), fish grow continuously throughout their lifespan and undergo a slightly different pattern of myogenesis involving a more prolonged hyperplasia (KOUMANS et al., 1991). The molecular events in the myogenic pathway are controlled by the MRFs, (MyoD, Myf-5, Myogenin and Mrf4) the expression of which regulates the timing of proliferation and differentiation (REHFELDT et al., 1999). The myogenic cells of mammalian, avian and fish embryos possess a level of developmental plasticity, whereby they can respond to the manipulation of various environmental conditions. Prenatal manipulation of temperature (MALTBY et al., 2004), nutrition (BAYOL et al., 2004), hormones (CLEMMONS, 1998) and innervation (LEFEUVRE et al., 1996) can have significant effects on the timing and length of the expression of the myogenic regulators, influencing the number of pre-natal muscle fibres and nuclei formed, and subsequently altering the adult muscle phenotype.

Nutrition Studies on intra-litter variation in the pig have shown that the nutritionally disadvantaged smallest fetus develop fewer secondary myofibres (in complete sections of M. semitendinosus) than the largest fetus that was well-nourished. However, primary fibre numbers are not affected (BEDI, 1982; WIGMORE and STICKLAND, 1983a). The difference in secondary myofibre numbers may be due to the reduced surface area of primary fibres (PENNEY et al., 1983; WIGMORE and STICKLAND, 1983b) in smaller fetuses, resulting from maternal undernutrition (MILLER et al., 1975; MADGEWICK, 1991; DWYER and STICKLAND, 1994) and/or uterine position (McLAREN and MICHIE, 1960; PERRY and ROWELL, 1969), therefore supporting less secondary fibres (WIGMORE and STICKLAND, 1983a). WIGMORE and STICKLAND (1983b) also showed that the larger fetuses contained more muscle DNA. A low fibre number predisposes the pig to poor long-term catch-up growth as shown by HANDEL and STICKLAND (1988).





The gestational time-point at which this undernutrition is targeted is critical for the development of secondary myofibres. Nutritional supplementation of pregnant sows from 2.5kg/day to 5kg/day during 25-50days of gestation (before the onset of secondary myofibre hyperplasia) enhanced the mean number of secondary myofibres by 9-13% in developing pig fetuses (DWYER et al., 1994), thus reducing the variation in myofibre development between the fetal size-range. A study of guinea pig offspring by DWYER et al., (1995) showed that feed restriction within the first half of gestation caused the same decrease in secondary myofibre number as feed restriction throughout gestation. Fetal muscle development is unaffected by late gestational maternal undernutrition as shown in a pig study (after 100 days gestation) by EZEKWE and OPOKU (1988).

A number of nutritional trials have shown an influence of prenatal nutrition on postnatal growth parameters without a significant influence on muscle fibre number in rats (BAYOL et al., 2004) and sheep (GREENWOOD et al., 1999; McCOARD et al., 2000). However, the myofibre number in sheep was differentially affected by season (McCOARD et al., 1997). In sheep, low levels of maternal nutrition resulted in fetuses with a higher connective tissue content (Figure 1), a factor that is also observed when intralitter comparisons are made in the pig (STICKLAND et al., 2000).

Fig. 1: A cross section of the semitendinosus muscle of control (left) and nutritionally restricted (right) sheep fetuses illustrating the higher amount of connective tissue in the restricted animal Temperature Different rearing temperatures can alter the cellularity of muscle tissue from fish embryos and larvae. In some fish species at hatch (e.g. Atlantic salmon; Salmo salar L.), higher incubation temperatures result in less but larger myofibres (Figure 2) and fewer nuclei in a complete larval cross-section compared to larvae reared at lower temperatures (STICKLAND et al., 1988; USHER et al., 1994). In herring embryos (Clupea harengus L.) a higher rearing temperature leads to more but smaller myofibres (VIEIRA and JOHNSTON, 1992). Muscle differentiation occurred later in rainbow trout (Oncorhynchus mykiss) embryos incubated at colder temperatures (XIE et al., 2001). This may indicate a longer proliferation phase which leads to more muscle fibres. Atlantic salmon reared at 5°C up to hatching grew significantly better posthatch, up to 3 weeks, than fish reared at 11°C. The post-hatch temperature was the same for all experimental salmon (NATHANAILIDES et al., 1995). Fish with more muscle fibres appear to grow faster in the first few weeks post-hatch. MATSCHAK et al. (1995) showed the importance of physiological hypoxia as a potential driving force behind the temperature effects on muscle development. These fish studies have demonstrated the importance of pre-hatch developmental temperature on pre- and post-hatch myogenesis and the implications these environmental alterations have on the growth potential of the fish. Fish grown at lower temperatures (near ambient level) not only have more and smaller myofibres, but they also have more nuclei thus suggesting increased capacity for hyperplasia and hypertrophy through a greater number of precursor cells.

Experiments with turkeys have shown that a small manipulation of incubation temperature (+/-1 to 2°C for 4 days during the early stages of incubation) can significantly alter the post-hatch muscle phenotype up to 3 weeks of age (MALTBY et al., 2004). The prenatal effects observed included an up-regulation of MyoD and PCNA, occurring during the period of secondary fibre formation. These changes in pre-hatch gene expression appeared to have an impact on post-hatch muscle development. An increase in fibre and nuclear number (Figure 3) was observed in the birds that underwent the temperature increase in early embryogenesis. The evidence in the turkey experiments suggest that increased muscle fibre number is associated with increased proliferation and delayed differentiation within the developing muscles.

–  –  –

Fig. 2: Total fibre number in a complete embryonic cross sectional area. The fish reared at 10oC have lower total muscle fibre numbers than those at the ambient temperature. Asterisk indicates a significant difference at P 0.05. (STICKLAND et al., 1988).

–  –  –

Fig. 3: The total fibre and nuclear number present in the cross sectional area of the semitendinosus muscle of 3week old turkeys exposed to 3 different temperatures between embryonic day 5 and embryonic day 8.

(MALTBY et al., 2004) Movement Stimulation of movement in ovo in chicken embryos has also yielded similar changes in the muscle phenotype. 4-aminopyridine administered during a key point in muscle development (i.e. myoblast proliferation) induces increased movement. Histological examination of the semitendinosus muscle revealed that fibre and nuclear number is greater in the stimulated embryos immediately pre-hatch compared to the control embryos (McENTEE et al., 2004). Also, higher level of succinic dehydrogenase activity (a marker of oxidative capacity) was observed immediately pre-hatch (embryonic day 20). The increase in muscle fibre and total nuclear number seen in the treated embryos is possibly as a result of a longer period of proliferation and may be due to a temporary suppression of myogenin (WALTERS et al., 2000; MALTBY et al., 2004). Initial results exploring how movement affects the temporal gene expression of key factors during myogenic proliferation and differentiation suggest that both the timing and level of expression of myogenin, myostatin and the IGFs is indeed altered by neuromuscular stimulation in ovo. The prolonged effects of 4-AP may also be attributable to the maintenance of polyneuronal innervation. Gene expression of neurogenic factors such as neural cell adhesion molecule (NCAM) and nicotinic acetylcholine receptor (nAChR) also appear to be significantly up-regulated in treated embryos during the later stages of embryogenesis (embryonic day 16 to 18). This suggests an increased level of innervation may be contributing to the observed increased proliferation.

Conclusions

The results of these experiments suggest that prenatal environmental factors (e.g.

temperature, maternal nutrition movement, uterine position) influence muscle development in a number of different ways. There may be an influence on the balance between proliferation and differentiation within given cell lineages (including secondary myofibres), which may also be affected by altered expression of IGFs, IGFBPs and IGF receptor and the timing of the expression of the myogenic regulatory factors. There may also be an influence on the commitment of early stem cells to particular lineages (i.e. muscle cells, satellite cells, side population cells and connective tissue cells) within developing muscles. The manipulation of these prenatal myogenic factors potentially has a fundamental role in the determination of meat quality and quantity in mammals, poultry and fish.

References

BAYOL, S., et al.:

The influence of undernutrition during gestation on skeletal muscle cellularity and on the expression of genes that control muscle growth. British Journal of Nutrition 91 (2004) 3, 331-339

BEDI, K.S., et al. :

Early life undernutrition in rats. 1. Quantitative histology of skeletal muscles from underfed young and refed adult animals. British Journal of Nutrition 47 (1982), 417-431.

CLEMMONS, D. R.:

Role of insulin-like growth factor binding proteins in controlling IGF actions. Molecular and Cellular Endocrinology 140 (1998), 19–24

DWYER, C.M.; STICKLAND, N.C.:

Supplementation of a restricted maternal diet with protein or carbohydrate alone prevents a reduction in fetal muscle fibre number in the guinea pig. British Journal of Nutrition 72 (1994), 173-180

DWYER, C.M., et al. :

The influence of maternal nutrition on muscle fibre number development in the porcine fetus and on subsequent postnatal growth. Journal of Animal Science 72 (1994), 911-917

DWYER, C.M., et al. :

Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guineapig. Reproduction Fertility and Development 7 (1995), 1285-1292

EZEKWE, M.O.; OPOKU, J.:

Postnatal response of liver and skeletal muscle in pigs from gestationally fasted gilts. Growth Development and Aging 52 (1998), 47-51

GREENWOOD P.L., et al.:

Intrauterine growth retardation is associated with reduced cell cycle activity, but not myofibre number, in ovine fetal muscle. Reproduction Fertility and Development 11 (1999) 4-5, 281-91

HANDEL, S.E.; STICKLAND, N.C.:

Catch-up growth in pigs: a relationship with muscle cellularity. Animal Production 47 (1998), 291-295



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