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University of Groningen the Rate of Living in Mice Vaanholt, Lobke Maria University of Groningen The rate of living in mice Vaanholt, Lobke Maria IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2007 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Vaanholt, L. M. (2007). The rate of living in mice: Impacts of activity and temperature on energy metabolism and longevity. s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 06-10-2021 The Rate of Living in Mice: Impacts of activity and temperature on energy metabolism and longevity The research reported in this thesis was carried out at the Behavioural Biology Group at the University of Groningen, The Netherlands and at the Rowett Institute in Aberdeen, Scotland. All studies were approved by the Ethical Committee of the University of Groningen (DEC 2777(-1), DEC 3039(-1), DEC 3128 and DEC 4184A). Production of this thesis was partly funded by the University of Groningen and the research school of Behavioural and Cognitive Neurosciences (BCN). Additional financial support came from UNO Roestvaststaal BV in Zevenaar and Harlan Netherlands BV in Horst. Cover: Lobke Vaanholt and Dick Visser Lay-out and figures: Dick Visser Photos: Lobke Vaanholt and Kristin Schubert Printed by: Ponsen en Looijen b.v., Wageningen ISBN: 9789036729444 ISBN: 9789036729451 (electronic version) RIJKSUNIVERSITEIT GRONINGEN The Rate of Living in Mice: Impacts of activity and temperature on energy metabolism and longevity PROEFSCHRIFT ter verkrijging van het doctoraat in de Wiskunde en Natuurwetenschappen aan de Rijksuniversiteit Groningen op gezag van de Rector Magnificus, dr. F. Zwarts, in het openbaar te verdedigen op vrijdag 23 maart 2007 om 16.15 uur door Lobke Maria Vaanholt geboren op 20 februari 1979 te Enschede Promotores: Prof. dr. S. Daan Prof. dr. G.H. Visser Beoordelingscommissie: Prof. dr. A.J.W. Scheurink Prof. dr. J.R. Speakman Prof. dr. R.J.G. Westendorp Contents Chapter 1 General introduction 7 Part I – ACTIVITY & METABOLISM Chapter 2 Wheel-running activity and energy metabolism in relation to ambient 19 temperature in mice selected for high wheel-running activity Chapter 3 Behavioural and physiological responses to increased foraging effort 35 in male mice Chapter 4 Plasma adiponectin is increased in mice selectively bred for 57 high wheel-running activity, but not by wheel running per se Chapter 5 Responses in energy balance to high-fat feeding in mice selectively-bred 71 for high wheel-running activity Part II – METABOLISM & AGEING Chapter 6 Life span, body composition, and metabolism in mice selected for 91 high wheel-running activity and their random-bred controls Chapter 7 Protein synthesis and antioxidant capacity in ageing mice: 111 effects of long-term voluntary exercise Chapter 8 Ageing under cold conditions: effects on body composition, 127 metabolism and longevity Chapter 9 Protein synthesis and antioxidant capacity in ageing mice: 147 effects of life-long cold exposure Chapter 10 General Perspective 161 References 177 List of abbreviations 193 Nederlandse samenvatting – Dutch summary 195 Addresses of co-authors 203 Dankwoord – Acknowledgements 205 Chapter1 General introduction 8 Chapter 1 “Death is the only certainty you have in life” In evolutionary biology, ageing is usually defined as a persistent decline in the age- specific fitness components of an organism due to internal physiological deteriora- tion. This definition integrates effects on reproduction and survival. Gerontologists simply define ageing as an increase in the likelihood that an individual will die in a certain time interval. As we age, intracellular processes degenerate and ultimately fail. This can lead to age-related diseases, such as cardiovascular disease, Parkin- son’s disease etc., and ultimately to death. There has been much speculation on the role of energy metabolism in the causation of these processes. This has led to the formation of several intriguing theories which attribute the causation of death ulti- mately to the very motor of life itself; the rate of living theory (Pearl, 1928; Rubner, 1908) and free radical theory of ageing (Harman, 1956). This idea was summarized by Murray (1926) in the statement: ‘If aliveness is measured by the velocity of chemical activity (heat production) an organism may in this sense be said to dig its own grave. The more abundant its manifestations of life, the greater will be its rate of senescence’. The primary aim of this thesis was to investigate the relationship between ageing and metabolic rate. In two large-scale experiments I manipulated the energy expen- diture of a group of animals by either increasing their physical activity or exposing them to cold. Survival curves were created for different experimental groups and I looked at changes that occurred in several physiological parameters that might be involved in ageing to explain differences that occurred in life span (Part II: Metabolism & Ageing). In addition, I explored the behavioural and physiological consequences of changes in energy balance in mice that had been selectively bred for high levels of spontaneous physical activity (Part I: Activity & Metabolism). ACTIVITY & METABOLISM Life history theory The evolution of life histories has been explained by the presence of limited resources that results in trade-offs between survival (maintenance of the body) and reproduction (Stearns, 2000). In times of plenty, resources can be allocated to growth and reproduction, but when resources are scarce, energy has to be allocated to enable survival of the individual and future success. In many species the repro- ductive season is tuned to coincide with the peak in food availability. When food is scarce, reproduction ceases and energy is allocated to increase the chance of sur- vival into the next year. There is a large variation in the way animals deal with such trade-offs. When there is a genetic basis for these decisions, natural selection favours life-history traits that result in a higher fitness. The main environmental General introduction 9 factors influencing the available resources for endothermic animals are environmen- tal temperature and food availability. In part I of this thesis we investigated the effects of low ambient temperatures or food availability on metabolism and the amount of voluntary activity mice were willing to engage. We used mice that had been selected by T. Garland Jr. for high wheel-running activity and their random-bred controls. Detailed description of the selection protocol and the main characteristics of these mice is provided in box 1.1. The amount of wheel-running activity was the selection criteria. After 31 genera- tions of selection the mice ran approximately 2,7 times as much as control animals (Rhodes et al., 2005). With the selection for wheel-running activity other traits have been co-selected (i.e. small body size) and much research has been undertaken to uncover these co-selected traits. In chapter 2 we investigate mice exposed to various ambient temperatures. We measured wheel-running activity and metabolic rate simultaneously to determine whether high-activity mice have evolved to have a lower running economy and whether they would more likely use heat generated by activity to substitute for thermoregulatory heat at low ambient temperatures than control mice do. In chap- ter 3 we manipulated food availability using a system in which animals had to run in a running wheel for a set number of revolutions to obtain a food pellets. This approach was used to study effects of food availability on physiological and behav- ioural responses in control and selected mice. Previous studies in rats by T. Adage showed that rats with low spontaneous levels of wheel-running activity have more difficulties to cope with a workload schedule than rats with high spontaneous levels of wheel-running activity. Similar effects were expected between control and high- activity mice. Exercise & obesity Obesity is becoming an increasingly prevalent health problem in affluent societies. It is often associated with metabolic derangements such as impaired glucose toler- ance, insulin resistance, high blood pressure, dyslipidemia, and abdominal obesity. When these metabolic abnormalities are displayed in concert (often referred to as the “metabolic syndrome”), they entail a high risk of developing into life-threaten- ing conditions such as cardiovascular disease and diabetes mellitus type 2 (for review see (Carroll and Dudfield, 2004; Moller and Kaufman, 2005)). Increased dietary fat intake in combination with a sedentary existence are factors precipitating the development of obesity and the associated metabolic syndrome. Adipose tissue produces several hormones, such as leptin and adiponectin, that are important for energy homeostasis. Levels of these hormones are associated with metabolic risk factors. Adiponectin levels are decreased and leptin levels increased in obese com- pared with lean subjects (Park et al., 2004). Mice that have been selected for high wheel-running activity (for detailed description see box 1.1.) have decreased levels of leptin even when correcting for fat mass (Girard et al., 2006).
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