Seasonal and fasting induced changes in iron metabolism in Djungarian hamsters

Abstract

Djungarian hamsters are small rodents that show pronounced physiological acclimations in response to changes in photoperiod, and unfavorable environmental conditions such as reduced food availability and low external temperature. These include substantial adjustments, such as severe body weight loss and the use of daily torpor. Torpor is a state of decreased physiological activity in eutherms, usually marked by low metabolic rate and a reduced body temperature. In this study, we investigated the effects of photoperiodic acclimation and food deprivation on systemic iron metabolism in Djungarian hamsters. Our study illustrates the association between liver iron levels and the incidence of torpor expression during the course of the experiment. Moreover, we show that both, acclimation to short photoperiods and long-term food restriction, associated with iron sequestration in the liver. This effect was accompanied with hypoferremia and mild reduction in the expression of principal iron-hormone, hepcidin. In addition to iron, the levels of manganese, selenium, and zinc were increased in the liver of hamsters under food restriction. These findings may be important factors for regulating physiological processes in hamsters, since iron and other trace elements are essential for many metabolic and physiological processes.

Fig 1. Scheme of animal experiment protocol in the present study.

First group of Djungarian hamsters (n = 17) was exposed to a short photoperiod (SP) with 8h light and 16h dark and received standard food ad libitum (AL). The second group of hamsters was subjected to a long photoperiod under ad libitum (LP; 16h light and 8h dark; n = 10) or subjected to food restriction (FR) for 5 weeks in a long photoperiod (LP; 16h light and 8h dark; n = 10). For the experimental details please refer to the Material and Methods.

Fig 2. Effect of photoperiodic changes on torpor incidence and hepatic iron levels in hamsters.

Djungarian hamsters were exposed to a long photoperiod ad libitum (LP-AL; 16h light and 8h dark; n = 10) or short photoperiod ad libitum (SP-AL; 8h light and 16h dark; n = 18). At the end of the experiments, hamsters were sacrificed and (A) Body weight (g), (B) Fur index and (C) torpor incidence (%) were measured. (D-E) Non-heme liver iron content, expressed in μg iron per gram dried liver tissue, was normalized to final body weight (BW) in both groups and correlated to body mass loss (%) in SP-AL group. (F-G) Non-heme iron content in the liver, expressed as μg iron per gram dried liver tissue, was normalized to final body weight (BW) in SP-AL groups with or without torpor expression (G) and correlated to the relative torpor incidence. All data are shown as mean ±SD. Statistically significant differences are indicated by p < .05 (*), p < .005 (***).

Fig 3. Effect of food restriction on torpor incidence and systemic iron levels.

(A) Djungarian hamsters were exposed to a long photoperiod (LP; 16h light and 8h dark) and subjected to either food restriction for 5 weeks (LP-FR, n = 10) or Ad libitim (LP-AL) (n = 10). At the end of the experiments, hamsters were sacrificed and (A) final body weight (g) and (B) The relative torpor incidence (%) were measured in both groups. (C-F) Non-heme iron content in the liver, expressed as μg iron per gram dried liver tissue, was normalized to final body weight (BW) and correlated to the expression of torpor and the percentage of body mass loss. (G-I) Plasma iron level (μg/dl) in LP-AL and LP-FR groups depending on the torpor expression and its correlation to body mass loss (%) in LP-FR group. All data are shown as mean ±SD. Statistically significant differences are indicated by p < .05 (*), p < .01 (**), p < .005 (***).

Fig 4. Effect of food restriction and torpor incidence on iron regulatory genes.

(A) Hepatic mRNA expression of (A, B) hepcidin (Hamp) and of (C, D) transferrin receptor 1 (Tfr1) were quantified by real-time PCR and normalized to 18S expression and to non-heme liver iron content. All data are shown as mean ±SD. Statistically significant differences are indicated by p < .05 (*), p < .01 (**).

Fig 5. Effect of food restriction on distribution of trace elements in the liver.

(A) The levels of (A,B) Manganese (Mn), (C,D) Selenium (Se), (E,F) Zinc (Zn), and (G,H) Copper (Cu) (ng/ gram liver tissues) were measured by TXRF and normalized to body weight (BW) of hamsters in LP-AL and LP-FR group, and depending on the torpor expression in the latter. All data are shown as mean ±SD. Statistically significant differences are indicated by p < .05 (*), p < .01 (**).