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INTRODUCTION
In mammals, lactation is the most energetically demanding period
of a female’s life and is characterized by a dramatic increase in the
energy and nutrient requirement of the organism for milk production
(Gutgesell et al., 2009). It is well known that several metabolic
adaptations occur in the different tissues of a lactating animal
(Williamson, 1980; Smith and Grove, 2002; Gutgesell et al., 2009).
For example, rates of fatty acid oxidation and ketogenesis, which
predominantly occur in the liver, are reduced during lactation and
this reduction helps to spare fatty acids for milk production in the
mammary gland (Whitelaw and Williamson, 1977). Reproduction
also requires particularly high levels of metabolism. In lactating
laboratory mice, for example, an elevated food intake as well as a
metabolic rate increase of 400% have been observed when compared
with non-reproductive mice (Hammond and Diamond, 1992;
Hammond, 1997; Cretegny and Genoud, 2006).
Although food consumption can increase dramatically during
lactation, a point is reached where this intake is maximized and
females appear unable, or unwilling, to increase their energy intake
any further (Speakman, 2008). Several theories have been put
forward to explain limits on the maximum rate at which animals
can ingest and expend energy (Hammond and Diamond, 1992;
Hammond et al., 1994; Speakman and Król, 2005; Speakman and
Król, 2010; Speakman and Król, 2011). The original ‘central
limitation’ hypothesis suggests a limitation in the capacity of the
alimentary tract to assimilate energy (including the liver), although
this has been refuted by several studies (Król and Speakman, 2003a;
Król and Speakman, 2003b; Król et al., 2003; Wu et al., 2009). The
‘peripheral limitation’ hypothesis states that the sustained energy
intake is set by the energy-consuming organs such as the mammary
glands during lactation (Hammond et al., 1994; Speakman and Król,
2005; Zhao and Cao, 2009; Speakman and Król, 2011; Zhao, 2011).
Alternatively, the ‘heat dissipation limit’ theory postulates that the
sustained energy intake is driven by the capacity of animals to
dissipate heat (Król and Speakman, 2003a; Król and Speakman,
2003b; Król et al., 2003; Speakman and Król, 2011).
Both hypotheses are likely to be important in all animals, but to
different extents (Speakman and Król, 2011; Zhao, 2011), and
suggest that energy intake and expenditure are central to the ability
of animals to reproduce. Additionally, the ‘saturated neural control’
hypothesis suggests that there may be limits in the ability of
peripheral signals such as leptin to stimulate factors in the brain
that regulate the intake of food, and contribute to energy intake
during lactation (Woodside et al., 2000; Mercer and Speakman,
2001; Denis et al., 2003; Speakman and Król, 2011). The abilities
of animals to increase metabolic rates and food intake have therefore
been fairly well investigated. However, the cellular changes that
occur during periods of high energy demand such as lactation have
received less attention.
Mitochondria are fundamental for energy production and their
ability to generate ATP in relation to tissue or cell demands could
potentially dictate reproductive investment. Cellular adaptation to
SUMMARY
Reproduction imposes significant costs and is characterized by an increased energy demand. As a consequence, individuals
adjust their cellular structure and function in response to this physiological constraint. Because mitochondria are central to
energy production, changes in their functional properties are likely to occur during reproduction. Such changes could cause
adjustments in reactive oxygen species (ROS) production and consequently in oxidative stress levels. In this study, we
investigated several mechanisms involved in energy production, including mitochondrial respiration at different steps of the
electron transport system (ETS) and related the results to citrate synthase activity in the liver of non-reproductive and
reproductive (two and eight pups) female house mice at peak lactation. Whereas we did not find differences between females
having different litter sizes, liver mitochondria of reproductive females showed lower ETS activity and an increase in
mitochondrial density when compared with the non-reproductive females. Although it is possible that these changes were due to
combined processes involved in reproduction and not to the relative investment in lactation, we propose that the mitochondrial
adjustment in liver might help to spare substrates and therefore energy for milk production in the mammary gland. Moreover, our
results suggest that these changes lead to an increase in ROS production that subsequently upregulates antioxidant defence
activity and decreases oxidative stress.
Key words: reproduction, metabolism, mitochondrial respiration, liver, citrate synthase.
Received 4 November 2012; Accepted 14 February 2013
The Journal of Experimental Biology 216, 2889-2895
© 2013. Published by The Company of Biologists Ltd
doi:10.1242/jeb.082685
RESEARCH ARTICLE
Physiological adaptations to reproduction. II. Mitochondrial adjustments in livers of
lactating mice
Nicolas Pichaud
1,2,
*, Michael Garratt
1
, J. William O. Ballard
2
and Robert C. Brooks
1
1
Evolution and Ecology Research Centre and School of Biological, Earth and Environmental Sciences, The University of New South
Wales, Sydney, New South Wales 2052, Australia and
2
School of Biotechnology and Biomolecular Sciences, The University of New
South Wales, Sydney, New South Wales 2052, Australia
*Author for correspondence (pichaud.nicolas@wanadoo.fr)
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