Effects of season and nutrition on growth hormone and insulin-like growth factor-I in male red deer

Abstract

GH and insulin-like growth factor (IGF)-I are important components of the growth axis. We undertook to determine how plasma levels of these hormones altered with different seasonal and nutritional states in young male red deer to provide an insight into how the growth axis changes under these conditions. Growth rate alters dramatically with season in male red deer, providing an opportunity to sample the same animals at two different growth rates within a short period of time. GH was measured every 15 min for 24 h in the fed state and after a 48-h fast, during slow growth in winter (23 June to 16 July), and during rapid growth in spring (8 September to 2 October). At the end of each sampling period, the animals were treated with N-methyl-D, L-aspartic acid (NMDA) (5 mg/kg live weight) and sampled for a further 1 h, 45 min. Glucose and IGF-I were measured hourly during each sampling period. Live weight was measured at weekly intervals. GH was secreted in a characteristic pattern in which pulses tended to occur in rapid succession, termed a volley, that was separated from the subsequent volley by a period of baseline GH levels, termed a latent period. There were more GH pulses/24 h in the fasted state than in the fed state in winter (12.4 vs. 7.8, standard error of the difference [SED] = 1.07, P < 0.001) and in spring (11.5 vs. 8.8, SED = 1.04, P < 0.05). The increased number of GH pulses in the fasted state could be attributed to a higher number of pulses per volley (winter = 3.7 vs. 2.5, SED = 0.16, P < 0.001; spring = 3.1 vs. 2.8, SED = 0.19). Consequently, the volleys were wider in the fasted state than the fed state (winter = 197 min vs. 122 min, SED = 25, P < 0.05; spring = 173 min vs. 154 min, SED = 24, P > 0.05), and the latent periods between volleys were shorter in the fasted state than the fed state (winter = 175 min vs. 280 min, SED = 14, P < 0.001; spring = 183 min vs. 262 min, SED = 11, P < 0.001). The main differences between seasons in the fed state were larger amplitude pulses (12.4 vs. 8.3 ng/ml, SED = 1.57, P < 0.05) and higher mean GH concentrations (4.1 vs. 2.3 ng/ml, SED = 0.44, P < 0.01) in spring than in winter. The number of volleys and the intravolley pulse interval did not change significantly with nutritional state or season. NMDA administration was followed by an increase in GH with higher GH levels found in the fed state than in the fasted state in both seasons. Fed animals also had a larger initial increase in GH (until 60 min post NMDA) than fasted animals in spring (P < 0.01). Plasma IGF-I was higher in the fed state than the fasted state in both winter (315 vs. 221 ng/ml, SED = 21.0, P < 0.001) and spring (651 vs. 494 ng/ml, SED = 37.5 P < 0.001) and in the fed state was higher in spring than in winter (SED = 29.1, P < 0.001). Blood glucose was higher in the fed state than fasted state in winter (6.1 vs. 5.5 mmol/l, SED = 0.07, P < 0.001) and there was a strong trend toward this same effect in spring although it did not reach statistical significance (6.0 vs. 5.7 mmol/l, SED = 0.26, P > 0.05). Growth rate in winter at 117 g/day was less than that in spring when 220 g/day was recorded (SED = 36.8, P < 0.05). These results demonstrate that the secretory pattern of GH and plasma IGF-I levels alter in response to changes in season and nutrition. The alterations in response to a 48-h fast show that the control of GH and IGF-I secretion may be rapid and is probably a response to maintain energy balance, whereas alterations with season reflect long term control that underlies the seasonal growth pattern of the animal.