Sex differences in physiological cardiac hypertrophy are associated with exercise-mediated changes in energy substrate availability.

Exercise-induced cardiac hypertrophy has been recently identified to be regulated in a sex-specific manner. In parallel, women exhibit enhanced exercise-mediated lipolysis compared with men, which might be linked to cardiac responses. The aim of the present study was to assess if previously reported sex-dependent differences in the cardiac hypertrophic response during exercise are associated with differences in cardiac energy substrate availability/utilization. Female and male C57BL/6J mice were challenged with active treadmill running for 1.5 h/day (0.25 m/s) over 4 wk. Mice underwent cardiac and metabolic phenotyping including echocardiography, small-animal PET, peri-exercise indirect calorimetry, and analysis of adipose tissue (AT) lipolysis and cardiac gene expression. Female mice exhibited increased cardiac hypertrophic responses to exercise compared with male mice, measured by echocardiography [percent increase in left ventricular mass (LVM): female: 22.2 ± 0.8%, male: 9.0 ± 0.2%; P < 0.05]. This was associated with increased plasma free fatty acid (FFA) levels and augmented AT lipolysis in female mice after training, whereas FFA levels from male mice decreased. The respiratory quotient during exercise was significantly lower in female mice indicative for preferential utilization of fatty acids. In parallel, myocardial glucose uptake was reduced in female mice after exercise, analyzed by PET {injection dose (ID)/LVM [%ID/g]: 36.8 ± 3.5 female sedentary vs. 28.3 ± 4.3 female training; P < 0.05}, whereas cardiac glucose uptake was unaltered after exercise in male counterparts. Cardiac genes involved in fatty acid uptake/oxidation in females were increased compared with male mice. Collectively, our data demonstrate that sex differences in exercise-induced cardiac hypertrophy are associated with changes in cardiac substrate availability and utilization.

[1]  M. Schwaiger,et al.  Gender differences in myocardial blood flow dynamics: lipid profile and hemodynamic effects. , 1999, Journal of the American College of Cardiology.

[2]  P. Herrero,et al.  Exercise training impacts the myocardial metabolism of older individuals in a gender-specific manner. , 2008, American journal of physiology. Heart and circulatory physiology.

[3]  E. Newsholme,et al.  The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. , 1963, Lancet.

[4]  Xianlin Han,et al.  The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. , 2002, The Journal of clinical investigation.

[5]  M. Kumari,et al.  Pnpla3/Adiponutrin deficiency in mice does not contribute to fatty liver disease or metabolic syndrome[S] , 2011, Journal of Lipid Research.

[6]  R. Zechner,et al.  Adipose triacylglycerol lipase deletion alters whole body energy metabolism and impairs exercise performance in mice. , 2009, American journal of physiology. Endocrinology and metabolism.

[7]  V. Regitz-Zagrosek,et al.  Erratum: Female sex and estrogen receptor-ß attenuate cardiac remodeling and apoptosis in pressure overload (American Journal of Physiology - Regulatory Integrative and Comparative Physiology (2010) 298 (R1597-R1606) DOI: 10.1152/ajpregu.00825.2009) , 2010 .

[8]  Sung-Cheng Huang,et al.  Noninvasive measurement of cardiovascular function in mice with high-temporal-resolution small-animal PET. , 2006, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[9]  L. Hellström,et al.  Gender Differences in Adremergic Regulation of Lipid Mobilization During Exercise , 1996, International journal of sports medicine.

[10]  Frank Eisenhaber,et al.  Fat Mobilization in Adipose Tissue Is Promoted by Adipose Triglyceride Lipase , 2004, Science.

[11]  E. Hirsch,et al.  Adaptive and maladaptive hypertrophic pathways: points of convergence and divergence. , 2004, Cardiovascular research.

[12]  M. Schwaiger,et al.  The relationship between myocardial blood flow and glucose uptake in ischemic canine myocardium determined with fluorine-18-deoxyglucose. , 1992, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[13]  R. Zechner,et al.  Hormone-sensitive Lipase Deficiency in Mice Causes Diglyceride Accumulation in Adipose Tissue, Muscle, and Testis* , 2002, The Journal of Biological Chemistry.

[14]  L. Leinwand,et al.  Sex modifies exercise and cardiac adaptation in mice. , 2004, American journal of physiology. Heart and circulatory physiology.

[15]  Bente Kiens,et al.  Skeletal muscle lipid metabolism in exercise and insulin resistance. , 2006, Physiological reviews.

[16]  M. Tarnopolsky,et al.  Substrate utilization during endurance exercise in men and women after endurance training. , 2001, American journal of physiology. Endocrinology and metabolism.

[17]  Role of muscle mass and mode of contraction in circulatory responses to exercise. , 1985, Journal of applied physiology.

[18]  G. Dorn The Fuzzy Logic of Physiological Cardiac Hypertrophy , 2007, Hypertension.

[19]  James A. Clark,et al.  Estrogen receptor-β mediates male-female differences in the development of pressure overload hypertrophy , 2005 .

[20]  J. Horowitz,et al.  Effect of gender on lipid kinetics during endurance exercise of moderate intensity in untrained subjects. , 2002, American journal of physiology. Endocrinology and metabolism.

[21]  D. Kelly,et al.  Fatty acid oxidation enzyme gene expression is downregulated in the failing heart. , 1996, Circulation.

[22]  H. Galbo,et al.  Expression profiling reveals differences in metabolic gene expression between exercise‐induced cardiac effects and maladaptive cardiac hypertrophy , 2005, The FEBS journal.

[23]  Godfrey L. Smith,et al.  Activation or inactivation of cardiac Akt/mTOR signaling diverges physiological from pathological hypertrophy , 2008, Journal of cellular physiology.

[24]  Louis Hue,et al.  The Randle cycle revisited: a new head for an old hat. , 2009, American journal of physiology. Endocrinology and metabolism.

[25]  J. Gustafsson,et al.  Estrogen Receptor-&bgr; Signals Left Ventricular Hypertrophy Sex Differences in Normotensive Deoxycorticosterone Acetate-Salt Mice , 2011, Hypertension.

[26]  E. Gilpin,et al.  Impact of anesthesia on cardiac function during echocardiography in mice. , 2002, American journal of physiology. Heart and circulatory physiology.

[27]  Stefan Neubauer,et al.  Sex‐specific characteristics of cardiac function, geometry, and mass in young adult elite athletes , 2006, Journal of magnetic resonance imaging : JMRI.

[28]  J C Stanley,et al.  The glucose-fatty acid cycle. Relationship between glucose utilization in muscle, fatty acid oxidation in muscle and lipolysis in adipose tissue. , 1981, British journal of anaesthesia.

[29]  D. Paterson,et al.  Novel quantitative phenotypes of exercise training in mouse models. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[30]  H. Taegtmeyer,et al.  Improved energy homeostasis of the heart in the metabolic state of exercise. , 2000, American journal of physiology. Heart and circulatory physiology.

[31]  J. Eckel,et al.  Induction of insulin resistance in primary cultured adult cardiac myocytes. , 1991, Endocrinology.

[32]  R. Hackam,et al.  Surface flashover of solid insulators in atmospheric air and in vacuum , 1985 .

[33]  F. Iellamo,et al.  Role of muscular factors in cardiorespiratory responses to static exercise: contribution of reflex mechanisms. , 1999, Journal of applied physiology.

[34]  J. Scheuer,et al.  Cardiac function in hypertrophied hearts from chronically exercised female rats. , 1981, Journal of applied physiology: respiratory, environmental and exercise physiology.

[35]  Sanjiv S. Gambhir,et al.  AMIDE: A Free Software Tool for Multimodality Medical Image Analysis , 2003 .

[36]  D. Redford,et al.  Direct effects of volatile anesthetics on cardiac functiona , 2008, Perfusion.

[37]  P. Buttrick,et al.  Physiologic, biochemical, and coronary adaptation to exercise conditioning. , 1987, Cardiology clinics.

[38]  L. Nybo,et al.  Adipose triglyceride lipase in human skeletal muscle is upregulated by exercise training. , 2009, American journal of physiology. Endocrinology and metabolism.

[39]  Wilfried Kindermann,et al.  Athlete's heart: right and left ventricular mass and function in male endurance athletes and untrained individuals determined by magnetic resonance imaging. , 2002, Journal of the American College of Cardiology.

[40]  Guenter Haemmerle,et al.  Lipolysis: pathway under construction , 2005, Current opinion in lipidology.

[41]  T. DeGrado,et al.  Validation of 18F-fluoro-4-thia-palmitate as a PET probe for myocardial fatty acid oxidation: effects of hypoxia and composition of exogenous fatty acids. , 2006, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.