Thermal manipulations in late-term chick embryos have immediate and longer term effects on myoblast proliferation and skeletal muscle hypertrophy

Abstract

We investigated the cellular and molecular bases for the promotion of muscle development and growth by temperature manipulations (TMs) during late-term chick embryogenesis. We show that incubation at 39.5 degrees C (increase of 1.7 degrees C from normal conditions) from embryonic days 16 to 18 (E16 to E18) for 3 or 6 h daily increased diameter of myofibers as of day 13 of age and enhanced absolute muscle growth relative to controls, until day 35 of age. TMs had immediate (E17) and later (up to 2 wk posthatch) effects in elevating muscle cell proliferation relative to controls. This was indicated by higher DNA incorporation of thymidine and a higher number of cells expressing PCNA in intact muscle, accompanied by higher Pax7 levels, all reflecting a higher number of myogenic cells, and suggesting that the increased hypertrophy can be attributed to a higher reservoir of myogenic progeny cells produced in response to the TM. IGF-I levels were higher in the TM groups than in controls, implying a mechanism by which heat manipulations in chicks affect muscle development, with locally secreted IGF-I playing a major role. Whereas hypertrophy was similar in both TM groups, cell proliferation and Pax7 levels were more robust in the 6-h muscle, mainly posthatch, suggesting a differential effect of various TM periods on cell reservoir vs. hypertrophy and a high sensitivity of myoblasts to relatively small changes in heat duration with respect to these processes, which is manifested in the short and long term.

Cyclic variations in incubation conditions induce adaptive responses to later heat exposure in chickens: a review

“…Improvement of embryo's heat thermotolerance has been the goal of many studies during recent decades (Iqbal et al, 1990;Piestun et al, 2008;Yahav, 2009;Druyan et al, 2012;Loyau et al, 2013). The hypothesis on which these studies were based highlighted the positive effects of increasing incubation temperature on the long-lasting improvement of thermotolerance.…”

“…Several studies have tested increases in incubation temperature before embryonic day 10 (E10; Yahav et al, 2004a;Collin et al, 2007;Piestun et al, 2008), during the phase before the adrenal axis regulating the stress response of animals is established. The period following E13 (2005) 39.6 E10 to E18 6 60% Collin et al (2007) 39.5 E8 to E10 and/or E16 to E18 3 65% Tona et al (2008) 39.5 E16 to E18 3 65% Piestun et al (2008 and 2009a) 39.5 E7 to E16 12, 24 65% Yalçin et al (2008) 38.5 E10 to E18 6 65% Tzschentke and Halle (2009) 38.2 to 38.4 E18 to E21 2, 24 -Molenaar et al (2011) 38.9 (egg shell) E7 to E19 24 50% Piestun et al (2011) 39.5 E7 to E16 12 65% Piestun et al (2013a) 39.5 E7 to E16 12 65% Loyau et al (2013) 39.5 E7 to E16 12 65% Walstra et al (2010) 40 E14 to E18 4 55% to 60% Willemsen et al (2010) 40.6 E16 to E18 4 30°C wb Al-Zhgoul et al (2013) 38.8 E10 to E18 6, 18 65% wb = wet bulb temperature, measurement of relative humidity in some incubators.…”

“…Second, the level of increase in incubation temperature during embryogenesis has to be accurately tuned. Thermal treatment during incubation of eggs has in many studies been based on repeated increases in incubation temperature up to 39.5°C to improve thermotolerance (v. 37.8°C; Moraes et al, 2004;Collin et al, 2007;Piestun et al, 2008;Loyau et al, 2013). A treatment temperature of 41°C appeared to be too high to maintain hatchability as good as in controls (Yahav et al, 2004a).…”

Increasing the incubation temperature between embryonic day 7 and 10 has no influence on the growth and slaughter characteristics as well as meat quality of broilers

“…A main advantage is that the embryonic development can be easily manipulated. Different endogenic factors with an impact on the avian embryogenesis have been investigated including the oxygen concentration (LeonVelarde and Monge, 2004;Chan and Burggren, 2005; -E-mail: Carsten.Werner@tiho-hannover.de Mortola and Labbe, 2005), the light colour (Rozenboim et al, 2003;Halevy et al, 2006) or the temperature around the brooding eggs (Christensen et al, 2001;Gauly et al, 2001;Von Blumroder and Tonhardt, 2002;Maltby et al, 2004;Tonhardt et al, 2004;Yahav et al, 2004a and2004b;Lourens et al, 2005;Collin et al, 2007;Hammond et al, 2007;Piestun et al, 2009). Direct manipulations include the in-ovo injection of growth hormones or factors (e.g.…”

“…embryonic day (ED) 4 to 7, ED 8 to 12, ED 8 to 10, ED 16 to 18) and sampling times before and after hatch of the animals (e.g. ED 18, 4 day, 25 day and 35 day post-hatch) (Maltby et al, 2004;Yahav et al, 2004a and2004b;Collin et al, 2007;Hammond et al, 2007;Piestun et al, 2009). Considering these publications -especially of this Maltby et al (2004) who showed that higher incubation temperatures between ED 9 and 12 in turkeys increases the MFN, the aim of this study was to investigate, how a higher incubation temperature between ED 7 and 10 -an important period of primary (embryonic) and secondary (foetal) myotube formation (Miller and Stockdale, 1986) -influences muscle development and/or structure in broiler post-hatch.…”