Physiological responses to chronic heat exposure in an aging non-human primate species, the gray mouse lemur (Microcebus murinus)
Graphical abstract
Research highlights
► Acclimation to summer prevented adult and aged mouse lemurs from normothermia impairment when exposed to heat exposure. ► Appropriate coping with heat exposure leads to maintenance of positive energy balance and unchanged water turnover. ► Aged mouse lemurs acclimated to winter showed severe normothermia impairment, leading to negative energy balance.
Introduction
The high prevalence for death in the elderly population during the last heat wave events in Europe (Sardon, 2007) points out the frailty of aged humans towards high ambient temperatures (Ta). Although hyperthermia risk in the elderly during heat waves is now considered a major public health problem (Kovats and Hajat, 2008), the intrinsic reasons for such impairment are still not well understood. Potential physiological failures, such as impaired cardiovascular capacities (Kenney and Munce, 2003) or increased risks of dehydration (Ferry, 2005) have been identified. The effects of global climate change could increase the probability of similar unpredictable heat waves in the future (Luber and McGeehin, 2008), so integrative studies on the responses to long-term heat exposure in the elderly are essential.
To better understand the effects of aging on homeostasis maintenance, we monitored the thermoregulatory responses of a highly photoperiod-responsive species, the gray mouse lemur (Microcebus murinus), during exposure to high Ta. This small nocturnal primate, originating from Madagascar, exhibits robust seasonal rhythms for most of its biological functions, i.e. body mass, body composition, energy metabolism and thermoregulatory capacities. As a result, reproduction is highly synchronized on photoperiod (PP) changes (Perret and Aujard, 2001), the mouse lemur being sexually active exclusively during long days (LD) which corresponds to the season for high food availability and high Ta (Dammhahn and Kappeler, 2008). Acclimation to short days (SD) leads to gonadal involution and metabolic depression, the animal facing food scarcity and low Ta (Dammhahn and Kappeler, 2008, Randrianambinina et al., 2003). In the gray mouse lemur under captive conditions, evidence exists for strong interactions between daily rhythms of core temperature (Tc) and photoperiod (Aujard et al., 1998), Ta (Aujard et al., 1998, Seguy and Perret, 2005, Terrien et al., 2008, Terrien et al., 2009b) and food availability (Giroud et al., 2008, Seguy and Perret, 2005). This nocturnal primate species [mean life span in captivity around 6 years (Perret, 1997)] has become popular during the past decade as a model of aging. Indeed, aging is associated in this species with decreased amplitude of the seasonal variations in body mass and gonadal hormones (Aujard and Perret, 1998), melatonin (Aujard et al., 2001), and DHEA-S (Perret and Aujard, 2005). Recent studies investigating the effects of cold exposure in the mouse lemur have showed differential effects of aging on thermoregulatory capacities and energy homeostasis according to photoperiod (Terrien et al., 2008, Terrien et al., 2009a, Terrien et al., 2009b). According to this, we hypothesized that responses to heat exposure could be impaired if the animals are not physiologically predisposed to respond to such stress. In the present integrative study, parameters of energy balance, such as energy intake and expenditure, locomotor activity (LA) levels, and water turnover were monitored in mouse lemurs exposed to chronic heat. Moreover, daily rhythms of Tc and LA are known to be impaired during aging (Van Someren et al., 2002, Weinert and Waterhouse, 2007) and were also analyzed. Finally, IGF-1 levels, previously described to be associated with longevity and stress resistance (Bonafe and Olivieri, 2009, Murakami, 2006), were measured. Physiological responses to heat stress were assessed in adult and aged mouse lemurs acclimated to LD photoperiod, i.e. physiologically predisposed to experiencing high Ta, and to SD, i.e. not predisposed to such heat exposure.
Section snippets
Animals and housing conditions
All gray mouse lemurs studied were males, born in the laboratory breeding colony of Brunoy (MNHN, France, license approval N° A91.114.1) and were pathogen free. General conditions of captivity were maintained constant: Ta (24–26 °C), relative humidity (55%). Food (including fresh fruits and a milky mixture) and water were available ad libitum. In captivity, seasonal variations of physiological functions are entrained by alternating 6-month periods of LD photoperiod (14 h of light / day) and SD
Tc levels increased after heat exposure
Heat exposure significantly modified daily Tc levels. Indeed, average values of Tc night, Tc day and Tc min increased between 25 and 34 °C, whatever age and photoperiod (Fig. 1 – Table 1). However, the observed increase was much higher in SD than in LD, leading to greater values of nocturnal and diurnal Tc levels at 34 °C during SD than during LD. During both LD and SD however, only adult mouse lemurs maintained general patterns of daily Tc rhythms at 34 °C and still exhibited a daily phase of Tc
Discussion
To our knowledge, this is the first study that investigates the effects of long-term chronic heat exposure, a fortiori in a non-human primate species. In particular, this work characterized the age-related impairment in energy homeostasis involved in the response to chronic heat and emphasizes the role of physiological plasticity as a major parameter for homeostasis maintenance. Efficient coping with high Ta was observed when the animals were physiologically predisposed to it, whatever the age.
Acknowledgments
This work was conducted with the financial support of the Institut de la Longévité et du Vieillissement, the Fondation pour la Recherche Médicale (FRM) and the ANR— Agence Nationale de la Recherche — The French National Research Agency under the Programme National de Recherche en Alimentation et nutrition humaine, project ANR-06-PNRA-010-01.
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