Naturally occurring compensated insulin resistance selectively alters glucose transporters in visceral and subcutaneous adipose tissues without change in AS160 activation

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1812, Issue 9, 2011, Pages 1098-1103

  Waller, A P ^a   Kohler, K ^a   Burns, T A ^a   Mudge, M C ^a   Belknap, J K ^a   Lacombe, V A ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Biotinylated photo affinity label; GLUT trafficking; GLUT12; Omental

Indexed keywords

GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 12; GLUCOSE TRANSPORTER 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOPSY TECHNIQUE; BIOTINYLATION; CELL SURFACE; CONTROLLED STUDY; FEMALE; GLUCOSE TRANSPORT; HORSE; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRAABDOMINAL FAT; INTRAVENOUS GLUCOSE TOLERANCE TEST; NONHUMAN; PHOSPHORYLATION; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBCUTANEOUS FAT; WESTERN BLOTTING;

ANIMALS; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; GLUCOSE TRANSPORTER TYPE 4; GTPASE-ACTIVATING PROTEINS; HORSES; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; SUBCUTANEOUS FAT;

ANIMALIA; EQUIDAE;

EID: 79960559552     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.02.007     Document Type: Article

References (42)

1. American Diabetes Association: Prediabetes FAQS. (2010). Available at Accessed 1/8/11. http://www.diabetes.org/diabetes-basics/prevention/pre-diabetes/pre-diabetes-faqs.html.
2. Ionut V., Liu H., Mooradian V., Castro A.V.B., Kabir M., Stefanovski D., Zheng D., Kirkman E.L., Bergman R.N. Novel canine models of obese pre-diabetes and of mild type 2 diabetes. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E38-E48.
3. Shepherd P.R., Kahn B.B. Glucose transporters and insulin action: implications for insulin resistance and diabetes mellitus. New. Engl. J. Med. 1999, 341:257-258.
4. Lee J., Xu Y., Lu L., Bergman B., Leitner J.W., Greyson C., Draznin B., Schwartz G.G. Multiple abnormalities of myocardial insulin signaling in a porcine model of diet-induced obesity. Am. J. Physiol. Heart Circ. Physiol. 2010, 298:H310-H319.
5. Frank N., Geor R.J., Bailey S.R., Durham A.E., Johnson P.J. Equine metabolic syndrome. J. Vet. Intern. Med. 2010, 24:467-475.
6. Freedland E.S. Role of a critical visceral adipose tissue threshold (CVATT) in metabolic syndrome: implications for controlling dietary carbohydrates: a review. Nutr. Metab. 2004, 1:1-24.
7. Cartwright M.J., Tchkonia T., Kirkland J.L. Aging in adipocytes: potential impact of inherent, depot-specific mechanisms. Exp. Geront. 2007, 42:463-471.
8. MacLaren R., Cui W., Simard S., Cianflone K. Influence of obesity and insulin sensitivity on insulin signaling genes in human omental and subcutaneous adipose tissue. J. Lipid Res. 2008, 49:308-323.
9. Bajzova M., Kovacikova M., Vitkova M., Climkakova E., Polak J., Kovacova Z., Viguerie N., Vedral T., Mikulasek L., Sramkova P., Srp A., Hejnova J., Langin D., Stich V. Retinol-binding protein 4 expression in visceral and subcutaneous fat in human obesity. Physiol. Res. 2008, 57:927-934.
10. Takahashi M., Eto M., Makino I. Peripheral insulin resistance precedes the onset of hyperglycemia in spontaneously diabetic Chinese hamsters of Asahikawa colony. Diabetes Res. Clin. Pract. 1993, 20:101-109.
11. Carvalho E., Jansson P.A., Axelsen M., Eriksson J.W., Huang X., Groop L., Rondinone C., Sjostrom L., Smith U. Low cellular IRS 1 gene and protein expression predict insulin resistance and NIDDM. FASEB J. 1999, 13:2173-2178.
12. Rogers S., Macheda M.L., Docherty S.E., Carty M.D., Henderson M.A., Soeller W.C., Gibbs E.M., James D.E., Best J.D. Identification of a novel glucose transporter-like protein-GLUT 12. Am. J. Physiol. Endocrinol. Metab. 2002, 282:E733-E738.
13. Stuart C.A., Howell M.A., Zhang Y., Yin D. Insulin-stimulated translocation of glucose transporter (GLUT) 12 parallels that of GLUT4 in normal muscle. J. Clin. Endocrinol. Metab. 2009, 94:3535-3542.
14. Sakamoto K., Holman G.D. Emerging role for AS160/TBC1D4 and TBC1D1 in the regulation of GLUT4 traffic. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E29-E37.
15. Muno J.D. Prevalence, risk factors and seasonality of plasma insulin concentrations in normal horses in central Ohio. MSc thesis 2009, The Ohio State University.
16. Burns T.A., Geor R.J., Mudge M.C., McCutcheon L.J., Hinchcliff K.W., Belknap J.K. Proinflammatory cytokine and chemokine gene expression profiles in subcutaneous and visceral adipose tissue depots of insulin-resistant and insulin-sensitive light breed horses. J. Vet. Intern. Med. 2010, 24:932-939.
17. A.P. Waller, T.A. Burns, M.C. Mudge, J.K. Belknap, V.A. Lacombe, Insulin resistance selectively alters cell surface glucose transporters, but not their protein expression, in equine skeletal muscle. J. Vet. Intern. Med. (2011) Epub Feb 11.
18. Hoffman R.M., Boston R.C., Stefanovski D., Kronfeld D.S., Harris P.A. Obesity and diet affect glucose dynamics and insulin sensitivity in Thoroughbred geldings. J. Anim. Sci. 2003, 81:2333-2342.
19. Ryder J.W., Yang J., Galuska D., Rincon J., Bjornholm M., Krook A., Lund S., Pedersen O., Wallberg-Henriksson H., Zierath J.R., Holman G.D. Use of a novel impermeable biotinylated photolabeling reagent to assess insulin- and hypoxia-stimulated cell surface GLUT4 content in skeletal muscle from type 2 diabetic patients. Diabetes 2000, 49:647-654.
20. Koumanov F., Yang J., Jones A.E., Hatanaka Y., Holman G.D. Cell-surface biotinylation of GLUT4 using bis-mannose photolabels. Biochem. J. 1998, 330:1209-1215.
21. Lacombe V.A., Hinchcliff K.W., Devor S.T. Effects of exercise and glucose administration on content of insulin-sensitive glucose-transporter in equine skeletal muscles. Am. J. Vet. Res. 2003, 64:1500-1506.
22. BLAST,BLAST protein sequence database. (2010) Available at: Accessed 5/21/2010. http://blast.ncbi.nlm.nih.gov/Blast.cgi.
23. Lundgren M., Buren J., Ruge T., Myrnas T., Eriksson J.W. Glucocorticoids down regulate glucose uptake capacity and insulin-signalling proteins in omental but not subcutaneous human adipocytes. J. Clin. Endocrinol. Metab. 2004, 89:2989-2997.
24. Laviola L., Perrini S., Cignarelli A., Natalicchi A., Leonardini A., De Stefano F., Cuscito M., De Fazio M., Memeo V., Neri V., Cignarelli M., Giorgino R., Giorgino F. Insulin signaling in human visceral and subcutaneous adipose tissue in vivo. Diabetes 2006, 55:952-961.
25. Cannon B., Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol. Rev. 2004, 84:277-359.
26. Ralston S.L., Nockels C.F., Squires E.L. Differences in diagnostic test results and hematologic data between aged and young horses. Am. J. Vet. Res. 1988, 49:1387-1392.
27. Geor R.J., Harris P.A. Dietary management of obesity and insulin resistance: countering risk for laminitis. Vet. Clin. Equine. 2009, 25:51-65.
28. Bergman R.N., Ader M., Huecking K., Citters G.V. Accurate assessment of β-cell function-the hyperbolic correction. Diabetes 2002, 51:S212.
29. Abel E.D., Peroni O., Kim J.K., Kim Y.B., Boss O., Hadro E., Minnemann T., Shulman G.I., Kahn B.B. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 2001, 409:729-733.
30. Gomez-Ruiz A.G., Milagro F.I., Campion J., Martinez J.A., Miguel C.D. Caveolin expression and activation in retroperitoneal and subcutaneous adipocytes: influence of a high fat diet. J. Cell. Physiol. 2010, 225:206-213.
31. Kelly K.R., Kashyap S.R., O'Leary V.B., Major J., Schauer P.R., Kirwan J.P. Retinol-binding protein 4 (RBP4) protein expression is increased in omental adipose tissue of severely obese patients. Obesity 2010, 18:663-666.
32. Garvey W.T., Maianu L., Zhu J.H., Hancock J.A., Golichowski A.M. Multiple defects in the adipocyte glucose transport system cause cellular insulin resistance in gestational diabetes: heterogeneity in the number and a novel abnormality in subcellular localization of GLUT4 glucose transporters. Diabetes 1993, 42:1773-1785.
33. Gollisch K.S., Brandauer J., Jessen N., Toyoda T., Nayer A., Hirshman M.F., Goodyear L.J. Effects of exercise training on subcutaneous and visceral adipose tissue in normal- and high-fat diet-fed rats. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E495-E504.
34. Carvalho E., Eliasson B., Wesslau C., Smith U. Impaired phosphorylation and insulin-stimulated translocation to the plasma membrane of protein kinase B/akt in adipocytes from Type II diabetic subjects. Diabetologia 2000, 43:1107-1115.
35. Maianu L., Keller S.R., Garvey W.T. Adipocytes exhibit abnormal subcellular distribution and translocation of vesicles containing glucose transporter 4 and insulin-regulated aminopeptidase in Type 2 Diabetes Mellitus: implications regarding defects in vesicle trafficking. J. Clin. Endocrinol. Metab. 2001, 86:5450-5456.
36. Drummond M.J., Bell J.A., Fujita S., Dreyer H.C., Glynn E.L., Volpi E., Rasmussen B.B. Resistance exercise increases human skeletal muscle AS160/TBC1D4 phosphorylation in association with enhanced leg glucose uptake during postexercise recovery. J. Appl. Physiol. 2008, 105:1967-1974.
37. Karlsson H.K.R., Zierath J.R., Kane S., Krook A., Lienhard G.E., Wallberg-Henriksson H. Insulin-stimulated phosphorylation of the akt substrate AS160 is impaired in skeletal muscle of type 2 diabetic subjects. Diabetes 2005, 54:1692-1697.
38. Lessard S.J., Rivas D.A., Chen Z., Bonen A., Febbraio M.A., Reeder D.W., Kemp B.E., Yaspelkis B.B., Hawley J.A. Tissue-specific effects of rosiglitazone and exercise in the treatment of lipid-induced insulin resistance. Diabetes 2007, 56:1856-1864.
39. Funai K., Cartee G.D. Inhibition of contraction-stimulated AMP-activated protein kinase inhibits contraction-stimulated increases in PAS-TBC1D1 and glucose transport without altering PAS-AS160 in rat skeletal muscle. Diabetes 2009, 58:1096-1104.
40. Bai L., Wang Y., Fan J., Chen Y., Ji W., Qu A., Xu P., James D.E., Xu T. Dissecting multiple steps of GLUT4 trafficking and identifying the sites of insulin action. Cell Metab. 2007, 5:47-57.
41. Huang S., Czech M.P. The GLUT4 glucose transporter. Cell Metab. 2007, 5:237-252.
42. Watson R.T., Pessin J.E. GLUT4 translocation: the last 200 nanometers. Cell. Signal. 2007, 19:2209-2217.