Evidence against a sexual dimorphism in glucose and fatty acid metabolism in skeletal muscle cultures from age-matched men and post-menopausal women

Acta Physiologica

Volumn 197, Issue 3, 2009, Pages 207-215

  Rune, A ^a   Salehzadeh, F ^a   Szekeres, F ^a   Kuhn I ^a   Osler, M E ^a   Al Khalili, L ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Glucose metabolism; Human; Lipid metabolism; MRNA gene expression; Sex differences

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ACYL COENZYME A DESATURASE; ADENOSINE PHOSPHATE; APOLIPOPROTEIN A1; APOLIPOPROTEIN A2; APOLIPOPROTEIN C2; APOLIPOPROTEIN C3; APOLIPOPROTEIN E; CARNITINE PALMITOYLTRANSFERASE I; GLUCOSE; GLUCOSE TRANSPORTER 4; GLYCOGEN; GLYCOGEN SYNTHASE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN; INSULIN; INTERLEUKIN 6; INTERLEUKIN 8; LOW DENSITY LIPOPROTEIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NERVE GROWTH FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE KINASE ISOZYME 4; SCATTER FACTOR; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 3;

ADULT; ARTICLE; BODY HEIGHT; BODY MASS; BODY WEIGHT; CELL GROWTH; CELL STRUCTURE; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FEMALE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOGEN SYNTHESIS; HEMOGLOBIN BLOOD LEVEL; HUMAN; HUMAN CELL; HUMAN TISSUE; INSULIN BLOOD LEVEL; LEUKOCYTE COUNT; LIPID OXIDATION; LIPOPROTEIN BLOOD LEVEL; MALE; MYOTUBE; ORAL GLUCOSE TOLERANCE TEST; POSTMENOPAUSE; PRIORITY JOURNAL; SEX DIFFERENCE; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; SYSTOLIC BLOOD PRESSURE; TISSUE CULTURE; TRIACYLGLYCEROL BLOOD LEVEL; VASTUS LATERALIS MUSCLE; WAIST CIRCUMFERENCE;

CELL CULTURE TECHNIQUES; FATTY ACIDS; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GLUCOSE; HUMANS; MALE; MIDDLE AGED; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; POSTMENOPAUSE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEX CHARACTERISTICS;

EID: 70350506336     PISSN: 17481708     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2009.02010.x     Document Type: Article

References (45)

1. Al-Khalili, L., Chibalin, A.V., Kannisto, K., Zhang, B.B., Permert, J., Holman, G.D., Ehrenborg, E., Ding, V.D.H., Zierath, J.R. Krook, A. 2003 Insulin action in cultured human skeletal muscle cells during differentiation: Assessment of cell surface GLUT4 and GLUT1 content. Cell Mol Life Sci 60, 991 998.
2. Al-Khalili, L., Kramer, D., Wretenberg, P. Krook, A. 2004. Human skeletal muscle cell differentiation is associated with changes in myogenic markers and enhanced insulin-mediated MAPK and PKB phosphorylation. Acta Physiol Scand 180, 395 403.
3. Benedict, F.G. Emmes, L.E. 1915. A comparison of the basal metabolism of normal men and women. J Biol Chem 20, 253 262.
4. Blaak, E. 2008. Sex differences in the control of glucose homeostasis. Curr Opin Clin Nutr Metab Care 11, 500 504.
5. Bonavaud, S., Thibert, P., Gherardi, R.K. Barlovatz-Meimon, G. 1997. Primary human muscle satellite cell culture: variations of cell yield, proliferation and differentiation rates according to age and sex of donors, site of muscle biopsy, and delay before processing. Biol Cell 89, 233 240.
6. Bouzakri, K., Zachrisson, A., Al-Khalili, L., Zhang, B.B., Koistinen, H.A., Krook, A. Zierath, J.R. 2006. siRNA-based gene silencing reveals specialized roles of IRS-1/Akt2 and IRS-2/Akt1 in glucose and lipid metabolism in human skeletal muscle. Cell Metab 4, 89 96.
7. Bray, G.A., Jablonski, K.A., Fujimoto, W.Y., Barrett-Connor, E., Haffner, S., Hanson, R.L., Hill, J.O., Hubbard, V., Kriska, A., Stamm, E. Pi-Sunyer, F.X. 2008. Relation of central adiposity and body mass index to the development of diabetes in the Diabetes Prevention Program. Am J Clin Nutr 87, 1212 1218.
8. Carter, S.L., Rennie, C. Tarnopolsky, M.A. 2001. Substrate utilization during endurance exercise in men and women after endurance training. Am J Physiol Endocrinol Metab 280, E898 E907.
9. Chen, S., Murphy, J., Toth, R., Campbell, D.G., Morrice, N.A. Mackintosh, C. 2008. Complementary regulation of TBC1D1 and AS160 by growth factors, insulin and AMPK activators. Biochem J 409, 449 459.
10. Cortright, R.N. Koves, T.R. 2000. Sex differences in substrate metabolism and energy homeostasis. Can J Appl Physiol 25, 288 311.
11. Deasy, B.M., Lu, A., Tebbets, J.C., Feduska, J.M., Schugar, R.C., Pollett, J.B., Sun, B., Urish, K.L., Gharaibeh, B.M., Cao, B., Rubin, R.T. Huard, J. 2007. A role for cell sex in stem cell-mediated skeletal muscle regeneration: female cells have higher muscle regeneration efficiency. J Cell Biol 177, 73 86.
12. Deasy, B.M., Schugar, R.C. Huard, J. 2008. Sex differences in muscle-derived stem cells and skeletal muscle. Crit Rev Eukaryot Gene Expr 18, 173 188.
13. Doumit, M.E., McFarland, D.C. Minshall, R.D. 1990. Satellite cells of growing turkeys: influence of donor age and sex on proliferation and differentiation in vitro. Exp Cell Res 189, 81 86.
14. Forsberg, A.M., Nilsson, E., Werneman, J., Bergstrom, J. Hultman, E. 1991. Muscle composition in relation to age and sex. Clin Sci (Lond) 81, 249 256.
15. Fredriksson, J., Anevski, D., Almgren, P., Sjogren, M., Lyssenko, V., Carlson, J., Isomaa, B., Taskinen, M.R., Groop, L. Orho-Melander, M. 2007. Variation in GYS1 interacts with exercise and gender to predict cardiovascular mortality. PLoS ONE 2, e285.
16. Frias, J.P., Macaraeg, G.B., Ofrecio, J., Yu, J.G., Olefsky, J.M. Kruszynska, Y.T. 2001. Decreased susceptibility to fatty acid-induced peripheral tissue insulin resistance in women. Diabetes 50, 1344 1350.
17. Goodpaster, B.H. Kelley, D.E. 1998. Role of muscle in triglyceride metabolism. Curr Opin Lipidol 9, 231 236.
18. Henry, R.R., Ciaraldi, T.P., Abrams-Carter, L., Mudaliar, S., Park, K.S. Nikoulina, S.E. 1996a. Glycogen synthase activity is reduced in cultured skeletal muscle cells of non-insulin-dependent diabetes mellitus subjects. Biochemical and molecular mechanisms. J Clin Invest 98, 1231 1236.
19. Henry, R.R., Ciaraldi, T.P., Mudaliar, S., Abrams, L. Nikoulina, S.E. 1996b. Acquired defects of glycogen synthase activity in cultured human skeletal muscle cells: influence of high glucose and insulin levels. Diabetes 45, 400 407.
20. Horton, T.J., Pagliassotti, M.J., Hobbs, K. Hill, J.O. 1998. Fuel metabolism in men and women during and after long-duration exercise. J Appl Physiol 85, 1823 1832.
21. Huang, S. Czech, M.P. 2007. The GLUT4 glucose transporter. Cell Metab 5, 237 252.
22. Huppertz, C., Fischer, B.M., Kim, Y.B., Kotani, K., Vidal-Puig, A., Slieker, L.J., Sloop, K.W., Lowell, B.B. Kahn, B.B. 2001. Uncoupling protein 3 (UCP3) stimulates glucose uptake in muscle cells through a phosphoinositide 3-kinase-dependent mechanism. J Biol Chem 276, 12520 12529.
23. Jensen, M.D. Johnson, C.M. 1996. Contribution of leg and splanchnic free fatty acid (FFA) kinetics to postabsorptive FFA flux in men and women. Metabolism 45, 662 666.
24. Kaseta, J.R., Skafar, D.F., Ram, J.L., Jacober, S.J. Sowers, J.R. 1999. Cardiovascular disease in the diabetic woman. J Clin Endocrinol Metab 84, 1835 1838.
25. Krotkiewski, M., Bjorntorp, P., Sjostrom, L. Smith, U. 1983. Impact of obesity on metabolism in men and women. Importance of regional adipose tissue distribution. J Clin Invest 72, 1150 1162.
26. Legato, M.J., Gelzer, A., Goland, R., Ebner, S.A., Rajan, S., Villagra, V. Kosowski, M. 2006. Gender-specific care of the patient with diabetes: review and recommendations. Gend Med 3, 131 158.
27. Mahlapuu, M., Johansson, C., Lindgren, K., Hjalm, G., Barnes, B.R., Krook, A., Zierath, J.R., Andersson, L. Marklund, S. (2004). Expression profiling of the [gamma]-subunit isoforms of AMP-activated protein kinase suggests a major role for [gamma]3 in white skeletal muscle. Am J Physiol Endocrinol Metab 286, E194 E200.
28. Matthews, D.R., Hosker, J.P., Rudenski, A.S., Naylor, B.A., Treacher, D.F. Turner, R.C. (1985). Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412 419.
29. McAinch, A.J., Steinberg, G.R., Mollica, J., O'Brien, P.E., Dixon, J.B., Macaulay, S.L., Kemp, B.E. Cameron-Smith, D. 2006. Differential regulation of adiponectin receptor gene expression by adiponectin and leptin in myotubes derived from obese and diabetic individuals. Obesity (Silver Spring) 14, 1898 1904.
30. McIntyre, E.A., Halse, R., Yeaman, S.J. Walker, M. 2004. Cultured muscle cells from insulin-resistant type 2 diabetes patients have impaired insulin, but normal 5-amino-4-imidazolecarboxamide riboside-stimulated, glucose uptake. J Clin Endocrinol Metab 89, 3440 3448.
31. Mercuro, G., Zoncu, S. Dragoni, F. 2003. Gender differences in cardiovascular risk factors. Ital Heart J 4, 363 366.
32. Moran, A., Jacobs, D.R., Jr., Steinberger, J., Steffen, L.M., Pankow, J.S., Hong, C.P. Sinaiko, A.R. 2008. Changes in insulin resistance and cardiovascular risk during adolescence: establishment of differential risk in males and females. Circulation 117, 2361 2368.
33. Muthusamy, T., Dhevika, S., Murugesan, P. Balasubramanian, K. 2007. Testosterone deficiency impairs glucose oxidation through defective insulin and its receptor gene expression in target tissues of adult male rats. Life Sci 81, 534 542.
34. Perseghin, G., Scifo, P., Pagliato, E., Battezzati, A., Benedini, S., Soldini, L., Testolin, G., Del Maschio, A. Luzi, L. 2001. Gender factors affect fatty acids-induced insulin resistance in nonobese humans: effects of oral steroidal contraception. J Clin Endocrinol Metab 86, 3188 3196.
35. Pinnamaneni, S.K., Southgate, R.J., Febbraio, M.A. Watt, M.J. 2006. Stearoyl CoA desaturase 1 is elevated in obesity but protects against fatty acid-induced skeletal muscle insulin resistance in vitro. Diabetologia 49, 3027 3037.
36. Regitz-Zagrosek, V., Lehmkuhl, E. Weickert, M.O. 2006. Gender differences in the metabolic syndrome and their role for cardiovascular disease. Clin Res Cardiol 95, 136 147.
37. Roden, M., Price, T.B., Perseghin, G., Petersen, K.F., Rothman, D.L., Cline, G.W. Shulman, G.I. 1996. Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 97, 2859 2865.
38. Roepstorff, C., Steffensen, C.H., Madsen, M., Stallknecht, B., Kanstrup, I.L., Richter, E.A. Kiens, B. 2002. Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects. Am J Physiol Endocrinol Metab 282, E435 E447.
39. Sato, K., Iemitsu, M., Aizawa, K. Ajisaka, R. 2008. Testosterone and DHEA activate the glucose metabolism-related signaling pathway in skeletal muscle. Am J Physiol Endocrinol Metab 294, E961 E968.
40. Simoneau, J.A. Bouchard, C. 1989. Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol 257, E567 E572.
41. Smadja, D., Cabre, P., May, F., Fanon, J.L., Rene-Corail, P., Riocreux, C., Charpentier, J.C., Fournerie, P., Saint-Vil, M. Ketterle, J. 2001. ERMANCIA: Epidemiology of Stroke in Martinique, French West Indies: Part I: methodology, incidence, and 30-day case fatality rate. Stroke 32, 2741 2747.
42. Tarnopolsky, L.J., MacDougall, J.D., Atkinson, S.A., Tarnopolsky, M.A. Sutton, J.R. 1990. Gender differences in substrate for endurance exercise. J Appl Physiol 68, 302 308.
43. Thompson, D.B., Pratley, R. Ossowski, V. 1996. Human primary myoblast cell cultures from non-diabetic insulin resistant subjects retain defects in insulin action. J Clin Invest 98, 2346 2350.
44. Welle, S., Tawil, R. Thornton, C.A. 2008. Sex-related differences in gene expression in human skeletal muscle. PLoS ONE 3, e1385.
45. Zierath, J.R. Wallberg-Henriksson, H. 2002. From receptor to effector: insulin signal transduction in skeletal muscle from type II diabetic patients. Ann N Y Acad Sci 967, 120 134.