Photoperiodic modulation of adrenal gland function in the rhesus macaque: effect on 24-h plasma cortisol and dehydroepiandrosterone sulfate rhythms and adrenal gland gene expression

Abstract

In temperate zones, day length changes markedly across the year, and in many mammals these photoperiodic variations are associated with physiological adaptations. However, the influence of this environmental variable on human behavior and physiology is less clear, and the potential underlying mechanisms are unknown. To address this issue, we examined the effect of changing photoperiods on adrenal gland function in ovariectomized female rhesus macaques (Macaca mulatta), both in terms of steroid hormone output and in terms of gene expression. The animals were sequentially exposed to the following lighting regimens, which were designed to simulate photoperiods associated with winter, spring/autumn and summer respectively: 8 h light:16 h darkness (short days), 12 h light:12 h darkness and 16 h light:8 h darkness (long days). Remote 24-h serial blood sampling failed to disclose any effect of photoperiod on mean or peak plasma levels of cortisol or dehydroepiandrosterone sulfate. However, there was a marked phase-advancement of both hormonal rhythms in short days, which was reflected as a similar phase-advancement of the daily motor activity rhythm. Gene microarray analysis of the adrenal gland transcriptome revealed photoperiod-induced differences in the expression of genes associated with homeostatic functions, including: development, lipid synthesis and metabolism, and immune function. Taken together, the results indicate that in primates, both circadian adrenal physiology and gene expression are influenced by seasonal changes in day length, which may have implications for adrenal-regulated physiology and behavior.

Figure 1

Effect of photoperiod on the 24-hour circulating (A) cortisol and (B) DHEAS rhythms in female rhesus macaques. Plasma samples were collected from the same animals after 10 weeks of exposure to each of the three photoperiods. Values are expressed as means ± SEM (N = 3). Note, the data are double plotted to aid visualization of circadian changes. Vertical dashed lines within each panel indicate the acrophases. The Vertical dashed line across all panels, indicate the beginning of the light phase. The horizontal white and black bars represent day and night, respectively.

Figure 2

Effect of photoperiod on motor activity in ovariectomized female rhesus macaques. (A) Left panels: Representative actograms from an individual animal that was exposed sequentially for 10 weeks to 8L:16D, 12L:12D and 16L:8D lighting regimens. Note, the activity data are double plotted to aid visualization of circadian changes. Right panels: Representative mean activity during the 10-week periods. The arrow indicates the advancement of activity onset, and the vertical dashed line indicates the beginning of the diurnal phase. The horizontal white and black bars indicate day and night, respectively. (B) Cosinor analysis was used to assess motor activity variables over each 10-week period. Comparisons were made using repeated-measures ANOVA followed by Bonferroni test. Values represent the means ± SEM from all three animals. *P<0.05, **P<0.01.

Figure 3

Effect of short days on adrenal gland gene expression. The gene microarrays were analyzed using the algorithm MAS 5.0. (A) Histogram depicting functional clustering of genes differentially regulated after exposure to short photoperiod. (B) Table of genes involved in development, lipid synthesis and metabolism and immune response, differentially expressed in 8L:16D vs. 12L:12D (P<0.05). Statistical comparisons were made by Students t-test.

Figure 4

Effect of long days on adrenal gland gene expression. The gene microarrays were analyzed using the algorithm MAS 5.0. (A) Histogram depicting functional clustering of genes differentially regulated after exposure to short photoperiod. (B) Table of genes involved in development, lipid synthesis and metabolism and immune response, differentially expressed in 16L:8D vs. 12L:12D (P<0.05). Statistical comparisons were made by Students t-test.

Figure 5

Expression levels for NCKAP1, FADS1, IL-11 and ACSL1, determined by Taqman qRT-PCR Values are expressed as means ± SEM (N = 3). Statistical comparisons were made by one way ANOVA, followed by Bonferroni test *P<0.05, **P<0.01.