Behavioral and physiologic responses to caloric restriction in mice

The purpose of the review is to highlight the influences of ambient temperature (T(a)) and caloric restriction (CR) on metabolism, cardiovascular function and behavior in mice. Standard vivarium ambient temperatures (T(a)?23 degrees C) are a mild cold stress for mice requiring elevated metabolic rate and food intake. Increasing T(a) into the zone of thermoneutrality (TMN?29-33 degrees C) markedly reduces food intake, metabolic rate, heart rate (HR) and blood pressure in mice. Mice are members of a diverse, yet unique group of homeothermic animals that respond to thermal and energetic challenges by allowing body temperature (T(b)) to fall to less than 31 degrees C, a condition known as torpor. In mice housed at standard T(a), torpor is induced by a single night of fasting or a few days of CR. The mechanisms responsible for initiating torpor are related to reduced caloric availability, but do not require leptin. Mice housed at TMN and subjected to CR exhibit physiologic reductions in metabolic rate and HR, but do not appear to enter torpor. Finally, mice exhibit differential locomotor activity responses during CR that depends on T(a). At standard T(a), mice display increased light-phase home-cage activity with CR. This response is virtually eliminated when CR is performed at TMN. We suggest that researchers using mice to investigate energy homeostasis and cardiovascular physiology carefully consider the influence of T(a) on physiology and behavior.

[1]  S. Swoap,et al.  Effect of ambient temperature on cardiovascular parameters in rats and mice: a comparative approach. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[2]  V. Viau,et al.  Starvation: early signals, sensors, and sequelae. , 1999, Endocrinology.

[3]  M. Maffei,et al.  Positional cloning of the mouse obese gene and its human homologue , 1994, Nature.

[4]  S. Tsai,et al.  Targeted gene regulation and gene ablation , 2001, Trends in Endocrinology & Metabolism.

[5]  I. Schmidt,et al.  Leptin selectively increases energy expenditure of food-restricted lean mice , 1998, International Journal of Obesity.

[6]  J. R. Nestler Relationships between Respiratory Quotient and Metabolic Rate during Entry to and Arousal from Daily Torpor in Deer Mice (Peromyscus maniculatus) , 1990, Physiological Zoology.

[7]  S. Woods,et al.  Signals that regulate food intake and energy homeostasis. , 1998, Science.

[8]  R. Henderson,et al.  Cardiovascular and metabolic responses to fasting and thermoneutrality in A y mice , 2003, Physiology & Behavior.

[9]  B. Metzger,et al.  The hypothermia of hypoglycemia. Studies with 2-deoxy-D-glucose in normal human subjects and mice. , 1972, The New England journal of medicine.

[10]  J B Chambers,et al.  Cardiovascular responses to caloric restriction and thermoneutrality in C57BL/6J mice. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[11]  M. Carroll,et al.  Overweight and obesity in the United States: prevalence and trends, 1960–1994 , 1998, International Journal of Obesity.

[12]  Christopher J. Gordon,et al.  Thermal biology of the laboratory rat , 1990, Physiology & Behavior.

[13]  J. Russell,et al.  Induction of voluntary prolonged running by rats. , 1987, Journal of applied physiology.

[14]  J. Silva The Thermogenic Effect of Thyroid Hormone and Its Clinical Implications , 2003, Annals of Internal Medicine.

[15]  I. Kettelhut,et al.  Increased sympathetic activity in rat white adipose tissue during prolonged fasting. , 1997, The American journal of physiology.

[16]  R. Cone,et al.  Genetic models of obesity and energy balance in the mouse. , 2000, Annual review of genetics.

[17]  M. Rashotte,et al.  Ingestive behavior and body temperature during the ovarian cycle in normotensive and hypertensive rats. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[18]  R. Leibel,et al.  Autonomic nervous system activity in weight gain and weight loss. , 1995, The American journal of physiology.

[19]  Z. Siegfried,et al.  Animal models in the investigation of anorexia , 2003, Physiology & Behavior.

[20]  G Heldmaier,et al.  Leptin suppresses semi-starvation induced hyperactivity in rats: implications for anorexia nervosa , 2000, Molecular Psychiatry.

[21]  K. Kanosue,et al.  Effects of food deprivation on daily changes in body temperature and behavioral thermoregulation in rats. , 2000, American journal of physiology. Regulatory, integrative and comparative physiology.

[22]  O. Stehling,et al.  Leptin reduces juvenile fat stores by altering the circadian cycle of energy expenditure. , 1996, The American journal of physiology.

[23]  J. Hudson SHALLOW, DAILY TORPOR: A THERMOREGULATORY ADAPTATION , 1978 .

[24]  W. Saris,et al.  Effects of energy restriction and exercise on the sympathetic nervous system. , 1995, International journal of obesity and related metabolic disorders : journal of the International Association for the Study of Obesity.

[25]  B. Janssen,et al.  Autonomic control of blood pressure in mice: basic physiology and effects of genetic modification. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[26]  G. P. Webb,et al.  Fasting-induced torpor in Mus musculus and its implications in the use of murine models for human obesity studies. , 1982, Comparative biochemistry and physiology. A, Comparative physiology.

[27]  J B Chambers,et al.  Cardiovascular and metabolic responses to fasting and thermoneutrality are conserved in obese Zucker rats. , 2001, American journal of physiology. Regulatory, integrative and comparative physiology.

[28]  Steven A. Thomas,et al.  Thermoregulatory and metabolic phenotypes of mice lacking noradrenaline and adrenaline , 1997, nature.

[29]  L. Landsberg,et al.  Suppression of sympathetic nervous system during fasting. , 1977, Science.

[30]  B. Beck KO's and organisation of peptidergic feeding behavior mechanisms , 2001, Neuroscience & Biobehavioral Reviews.

[31]  J. Hebebrand,et al.  Hyperactivity in patients with anorexia nervosa and in semistarved rats: evidence for a pivotal role of hypoleptinemia , 2003, Physiology & Behavior.

[32]  J. Himms-Hagen,et al.  Raising at thermoneutrality prevents obesity and hyperphagia in BAT-ablated transgenic mice. , 1997, The American journal of physiology.

[33]  L. D. Carlson,et al.  Glossary of Terms for Thermal Physiology. Glossary of Terms for Thermal Physiology' Members Uf International Commission for Thermal Physiohgy Sv&zv3 , 2012 .

[34]  J. Hudson,et al.  Daily Torpor in the Laboratory Mouse, Mus musculus Var. Albino , 1979, Physiological Zoology.

[35]  J. R. Nestler,et al.  Relationships between body temperature, thermal conductance,Q10 and energy metabolism during daily torpor and hibernation in rodents , 2004, Journal of Comparative Physiology B.

[36]  L. Landsberg,et al.  Caloric restriction lowers blood pressure in the spontaneously hypertensive rat. , 1978, Metabolism: clinical and experimental.

[37]  Td Williams,et al.  Diet‐induced obesity and cardiovascular regulation in C57BL/6J mice , 2003, Clinical and experimental pharmacology & physiology.

[38]  J. Hall,et al.  Obesity-induced hypertension. Renal function and systemic hemodynamics. , 1993, Hypertension.

[39]  M. Picciotto,et al.  Using knockout and transgenic mice to study neurophysiology and behavior. , 1998, Physiological reviews.

[40]  R. Henderson,et al.  Concurrent reductions in blood pressure and metabolic rate during fasting in the unrestrained SHR. , 2000, American journal of physiology. Regulatory, integrative and comparative physiology.

[41]  J. E. Morhardt Heart rates, breathing rates and the effects of atropine and acetylcholine on white-footed mice (Peromyscus sp.) during daily torpor. , 1970, Comparative biochemistry and physiology.

[42]  R. Boakes,et al.  Activity-based anorexia: Ambient temperature has been a neglected factor , 2002, Psychonomic bulletin & review.

[43]  G. Körtner,et al.  Leptin increases energy expenditure of a marsupial by inhibition of daily torpor. , 1998, The American journal of physiology.

[44]  J. Himms-Hagen,et al.  Temperature-dependent feeding: lack of role for leptin and defect in brown adipose tissue-ablated obese mice. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[45]  Ralph H. Johnson THERMOREGULATION AND BIOENERGETICS , 1976 .

[46]  S. Swoap Altered leptin signaling is sufficient, but not required, for hypotension associated with caloric restriction. , 2001, American journal of physiology. Heart and circulatory physiology.

[47]  E. Ravussin,et al.  Calorie restriction and aging: review of the literature and implications for studies in humans. , 2003, The American journal of clinical nutrition.

[48]  C. Berul Electrophysiological phenotyping in genetically engineered mice. , 2003, Physiological genomics.

[49]  R. Davisson,et al.  Long-term telemetric measurement of cardiovascular parameters in awake mice: a physiological genomics tool. , 2001, Physiological genomics.

[50]  H. Ehmke Mouse gene targeting in cardiovascular physiology. , 2003, American journal of physiology. Regulatory, integrative and comparative physiology.

[51]  M. Rashotte,et al.  Central Leptin Infusion Attenuates the Cardiovascular and Metabolic Effects of Fasting in Rats , 2001, Hypertension.

[52]  I. Zucker,et al.  Reduced glucose availability induces torpor in Siberian hamsters. , 1994, The American journal of physiology.

[53]  R W Hart,et al.  Effect of chronic caloric restriction on the circadian regulation of physiological and behavioral variables in old male B6C3F1 mice. , 1990, Chronobiology international.

[54]  R. Weindruch,et al.  Calorie restriction lowers body temperature in rhesus monkeys, consistent with a postulated anti-aging mechanism in rodents. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[55]  G F Cahill,et al.  Starvation in man. , 1970, The New England journal of medicine.

[56]  P. Ernsberger,et al.  Effects of fasting and refeeding on blood pressure are determined by nutritional state, not by body weight change. , 1988, American journal of hypertension.

[57]  Ronald W. Hart,et al.  Effect of chronic caloric restriction on physiological variables related to energy metabolism in the male Fischer 344 rat , 1989, Mechanisms of Ageing and Development.

[58]  B. Sauer Inducible gene targeting in mice using the Cre/lox system. , 1998, Methods.

[59]  J. Himms-Hagen,et al.  Food restriction increases torpor and improves brown adipose tissue thermogenesis in ob/ob mice. , 1985, The American journal of physiology.

[60]  T. Nagy,et al.  Strain variation in the response of body temperature to dietary restriction , 2003, Mechanisms of Ageing and Development.

[61]  L. Leon,et al.  Torpor in mice is induced by both leptin-dependent and -independent mechanisms. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[62]  J. Dark,et al.  Metabolic Fuel Availability Influences Thermoregulation in Deer Mice (Peromyscus maniculatus) , 1997, Physiology & Behavior.

[63]  J. E. Schneider,et al.  Control of fertility by metabolic cues. , 1996, The American journal of physiology.

[64]  Christopher J. Gordon,et al.  Temperature Regulation in Laboratory Rodents , 1993 .

[65]  E. Rappaport,et al.  Initiation, duration and dissipation of diet-induced changes in sympathetic nervous system activity in the rat. , 1982, Metabolism: clinical and experimental.