Fetuin-A is linked to improved glucose tolerance after short-term exercise training in nonalcoholic fatty liver disease.

Fetuin-A is synthesized in the liver and may be associated with nonalcoholic fatty liver disease (NAFLD) and type 2 diabetes. Lifestyle-induced weight loss reduces fetuin-A, but the effect of exercise alone is unknown. We determined the effect of short-term exercise training on plasma fetuin-A in 13 (50.5 ± 3.4 yr) obese adults (body mass index, 33.3 ± 0.9 kg/m(2)) with clinically diagnosed NAFLD. Subjects participated in 7 days of supervised exercise training (60 min/day at ∼85% maximum heart rate) and were instructed to maintain their normal caloric and macronutrient intake. Insulin resistance was assessed by an oral glucose tolerance test. Hepatic triglyceride content (HTGC) was determined by proton MRI. We used C2C12 skeletal muscle cells to examine the direct effect of fetuin-A on 2-deoxyglucose uptake, insulin signaling [phosphorylation of Akt and AS160 (pAkt and pAS160, respectively)], and glucose transporter-4 (GLUT-4) translocation. Insulin resistance was reduced by 29% (P < 0.05), and glucose area under the curve (AUC) was decreased by 13% (P < 0.01) after the 7 days of exercise. Furthermore, circulating fetuin-A was decreased by 11% (4.2 ± 03 vs. 3.6 ± 0.2 nM; P < 0.02), and this change correlated with reduced insulin resistance (r = 0.62; P < 0.04) and glucose AUC (r = 0.58; P < 0.04). Importantly, the exercise program did not change body weight (P = 0.12), HTGC (P = 0.73), or aerobic capacity (P = 0.14). In vitro experiments revealed that fetuin-A decreased skeletal muscle glucose uptake by downregulating pAkt and pAS160 and subsequent GLUT-4 translocation to the plasma membrane. Together, our findings highlight a role for fetuin-A in skeletal muscle insulin resistance and suggest that part of the exercise-induced improvement in glucose tolerance in patients with NAFLD may be due to lowering fetuin-A.

[1]  S. Mukhopadhyay,et al.  Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance , 2012, Nature Medicine.

[2]  C. Flask,et al.  Short-term exercise reduces markers of hepatocyte apoptosis in nonalcoholic fatty liver disease. , 2012, Journal of applied physiology.

[3]  H. Ou,et al.  Endoplasmic reticulum stress induces the expression of fetuin-A to develop insulin resistance. , 2012, Endocrinology.

[4]  R. Rector,et al.  Does physical inactivity cause nonalcoholic fatty liver disease? , 2011, Journal of applied physiology.

[5]  H. J. Yoo,et al.  Effects of a three‐month combined exercise programme on fibroblast growth factor 21 and fetuin‐A levels and arterial stiffness in obese women , 2011, Clinical endocrinology.

[6]  H. Ou,et al.  Serum fetuin‐A concentrations are elevated in subjects with impaired glucose tolerance and newly diagnosed type 2 diabetes , 2011, Clinical endocrinology.

[7]  J. Hagberg,et al.  Plasma fetuin-A concentrations in young and older high- and low-active men. , 2011, Metabolism: clinical and experimental.

[8]  M. Fasshauer,et al.  Adipokine Pattern in Subjects with Impaired Fasting Glucose and Impaired Glucose Tolerance in Comparison to Normal Glucose Tolerance and Diabetes , 2010, PloS one.

[9]  G. Schernthaner,et al.  Elevated Fetuin-A concentrations in morbid obesity decrease after dramatic weight loss. , 2010, The Journal of clinical endocrinology and metabolism.

[10]  Enzo Bonora,et al.  Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. , 2010, The New England journal of medicine.

[11]  S. Mukhopadhyay,et al.  NF-kappaB mediates lipid-induced fetuin-A expression in hepatocytes that impairs adipocyte function effecting insulin resistance. , 2010, The Biochemical journal.

[12]  D. Reboussin,et al.  Effect of a 12-Month Intensive Lifestyle Intervention on Hepatic Steatosis in Adults With Type 2 Diabetes , 2010, Diabetes Care.

[13]  N. Stefan,et al.  The effect of 6-weeks of aerobic exercise training on serum fetuin-A levels in non-diabetic obese women. , 2010, Experimental and clinical endocrinology & diabetes : official journal, German Society of Endocrinology [and] German Diabetes Association.

[14]  S. Klein,et al.  Diet and Exercise Interventions Reduce Intrahepatic Fat Content and Improve Insulin Sensitivity in Obese Older Adults , 2009, Obesity.

[15]  S. Cummings,et al.  Fetuin-A and change in body composition in older persons. , 2009, The Journal of clinical endocrinology and metabolism.

[16]  G. Cartee,et al.  Exercise and Insulin: Convergence or Divergence at AS160 and TBC1D1? , 2009, Exercise and sport sciences reviews.

[17]  Y. Ikeda,et al.  High glucose induces transactivation of the alpha2-HS glycoprotein gene through the ERK1/2 signaling pathway. , 2009, Journal of atherosclerosis and thrombosis.

[18]  M. Staten,et al.  Effects of 7 days of exercise training on insulin sensitivity and responsiveness in type 2 diabetes mellitus. , 2009, American journal of physiology. Endocrinology and metabolism.

[19]  T. Reinehr,et al.  Fetuin-A and its relation to metabolic syndrome and fatty liver disease in obese children before and after weight loss. , 2008, The Journal of clinical endocrinology and metabolism.

[20]  M. Schulze,et al.  Plasma Fetuin-A Levels and the Risk of Type 2 Diabetes , 2008, Diabetes.

[21]  H. Koyama,et al.  Effects of pioglitazone on serum fetuin-A levels in patients with type 2 diabetes mellitus. , 2008, Metabolism: clinical and experimental.

[22]  Annemarie Koster,et al.  Fetuin-A and incident diabetes mellitus in older persons. , 2008, JAMA.

[23]  R. DeFronzo,et al.  Adipocytes in subjects with impaired fasting glucose and impaired glucose tolerance are resistant to the anti-lipolytic effect of insulin , 2008, Acta Diabetologica.

[24]  Norbert Stefan,et al.  Causes and metabolic consequences of Fatty liver. , 2008, Endocrine reviews.

[25]  G. Grunberger,et al.  Fetuin-null mice are protected against obesity and insulin resistance associated with aging. , 2006, Biochemical and biophysical research communications.

[26]  J. Kirwan,et al.  Exercise-induced reversal of insulin resistance in obese elderly is associated with reduced visceral fat. , 2006, Journal of applied physiology.

[27]  F. Schick,et al.  α2-Heremans-Schmid Glycoprotein/ Fetuin-A Is Associated With Insulin Resistance and Fat Accumulation in the Liver in Humans , 2006 .

[28]  A. McCullough Pathophysiology of nonalcoholic steatohepatitis. , 2006, Journal of clinical gastroenterology.

[29]  Y. Tamura,et al.  Effects of diet and exercise on muscle and liver intracellular lipid contents and insulin sensitivity in type 2 diabetic patients. , 2005, The Journal of clinical endocrinology and metabolism.

[30]  Jonathan C. Cohen,et al.  Prevalence of hepatic steatosis in an urban population in the United States: Impact of ethnicity , 2004, Hepatology.

[31]  G. Grunberger,et al.  Improved insulin sensitivity and resistance to weight gain in mice null for the Ahsg gene. , 2002, Diabetes.

[32]  J. C. Ho,et al.  Mössbauer studies of melt-spun Pr2Fe14B ribbons , 2001 .

[33]  E. Evans,et al.  Effects of HRT and exercise training on insulin action, glucose tolerance, and body composition in older women. , 2001, Journal of applied physiology.

[34]  D. O'Gorman,et al.  Regular exercise enhances insulin activation of IRS-1-associated PI3-kinase in human skeletal muscle. , 2000, Journal of applied physiology.

[35]  K. Claffey,et al.  TNF-alpha impairs insulin signaling and insulin stimulation of glucose uptake in C2C12 muscle cells. , 1999, The American journal of physiology.

[36]  K. Claffey,et al.  TNF-α impairs insulin signaling and insulin stimulation of glucose uptake in C2C12muscle cells. , 1999, American journal of physiology. Endocrinology and metabolism.

[37]  G. Bray,et al.  Differential expression of insulin receptor tyrosine kinase inhibitor (fetuin) gene in a model of diet-induced obesity. , 1998, Life sciences.

[38]  J. Ivy,et al.  Effects of exercise training on muscle GLUT-4 protein content and translocation in obese Zucker rats. , 1993, The American journal of physiology.

[39]  C. Slentz,et al.  Glucose transporters and maximal transport are increased in endurance-trained rat soleus. , 1992, Journal of applied physiology.

[40]  Y. Mitsumoto,et al.  Development regulation of the subcellular distribution and glycosylation of GLUT1 and GLUT4 glucose transporters during myogenesis of L6 muscle cells. , 1992, The Journal of biological chemistry.

[41]  P. Neufer,et al.  Elevated skeletal muscle glucose transporter levels in exercise-trained middle-aged men. , 1991, The American journal of physiology.

[42]  W. M. Sherman,et al.  Exercise training increases glucose transporter protein GLUT‐4 in skeletal muscle of obese Zucker (fa/fa) rats , 1990, FEBS letters.

[43]  G. Pagès,et al.  Characterization of a natural inhibitor of the insulin receptor tyrosine kinase: cDNA cloning, purification, and anti-mitogenic activity , 1989, Cell.

[44]  R. Turner,et al.  Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man , 1985, Diabetologia.

[45]  K. Frayn,et al.  Calculation of substrate oxidation rates in vivo from gaseous exchange. , 1983, Journal of applied physiology: respiratory, environmental and exercise physiology.