Activation of phosphatidylinositol-3 kinase, AMP-activated kinase and Akt substrate-160 kDa by trans-10, cis-12 conjugated linoleic acid mediates skeletal muscle glucose uptake

Journal of Nutritional Biochemistry

Volumn 24, Issue 2, 2013, Pages 445-456

  Mohankumar, Suresh K ^a,b   Taylor, Carla G ^a,b   Siemens, Linda ^a,b   Zahradka, Peter ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b ST BONIFACE GENERAL HOSPITAL   (Canada)

Author keywords

CLA isomers; Glucose uptake; GLUT4 translocation; Signal transduction; Skeletal muscle

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; GLUCOSE TRANSPORTER 4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LINOLEIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P85;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GLUCOSE TRANSPORT; MYOTUBE; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; SKELETAL MUSCLE;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL MEMBRANE; DRUG SYNERGISM; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; GTPASE-ACTIVATING PROTEINS; INSULIN; LINOLEIC ACIDS, CONJUGATED; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RIBONUCLEOTIDES;

EID: 84872825629     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.01.006     Document Type: Article

References (58)

1. Katz L.D., Glickman M.G., Rapoport S., Ferrannini E., DeFronzo R.A. Splanchnic and peripheral disposal of oral glucose in man. Diabetes 1983, 32:675-679.
2. Goodyear L.J., Hirshman M.F., Napoli R., Calles J., Markuns J.F., Ljungqvist O., et al. Glucose ingestion causes GLUT4 translocation in human skeletal muscle. Diabetes 1996, 45:1051-1056.
3. Wijesekara N., Tung A., Thong F., Klip A. Muscle cell depolarization induces a gain in surface GLUT4 via reduced endocytosis independently of AMPK. Am J Physiol Endocrinol Metab 2006, 290:E1276-E1286.
4. Leney S.E., Tavare J.M. The molecular basis of insulin-stimulated glucose uptake: signalling, trafficking and potential drug targets. J Endocrinol 2009, 203:1-18.
5. Bouzakri K., Koistinen H.A., Zierath J.R. Molecular mechanisms of skeletal muscle insulin resistance in type 2 diabetes. Curr Diabetes Rev 2005, 1:167-174.
6. Bjornholm M., Zierath J.R. Insulin signal transduction in human skeletal muscle: identifying the defects in Type II diabetes. Biochem Soc Trans 2005, 33:354-357.
7. Kritchevsky D. Antimutagenic and some other effects of conjugated linoleic acid. Br J Nutr 2000, 83:459-465.
8. Banni S. Conjugated linoleic acid metabolism. Curr Opin Lipidol 2002, 13:261-266.
9. Pariza M.W., Park Y., Cook M.E. Conjugated linoleic acid and the control of cancer and obesity. Toxicol Sci 1999, 52:107-110.
10. Kennedy A., Martinez K., Schmidt S., Mandrup S., LaPoint K., McIntosh M. Antiobesity mechanisms of action of conjugated linoleic acid. J Nutr Biochem 2010, 21:171-179.
11. Ryder J.W., Portocarrero C.P., Song X.M., Cui L., Yu M., Combatsiaris T., et al. Isomer-specific antidiabetic properties of conjugated linoleic acid. Improved glucose tolerance, skeletal muscle insulin action, and UCP-2 gene expression. Diabetes 2001, 50:1149-1157.
12. Henriksen E.J., Teachey M.K., Taylor Z.C., Jacob S., Ptock A., Kramer K., et al. Isomer-specific actions of conjugated linoleic acid on muscle glucose transport in the obese Zucker rat. Am J Physiol Endocrinol Metab 2003, 285:E98-E105.
13. Moloney F., Toomey S., Noone E., Nugent A., Allan B., Loscher C.E., et al. Antidiabetic effects of cis-9, trans-11-conjugated linoleic acid may be mediated via anti-inflammatory effects in white adipose tissue. Diabetes 2007, 56:574-582.
14. Noto A., Zahradka P., Ryz N.R., Yurkova N., Xie X., Taylor C.G. Dietary conjugated linoleic acid preserves pancreatic function and reduces inflammatory markers in obese, insulin-resistant rats. Metabolism 2007, 56:142-151.
15. Noto A., Zahradka P., Yurkova N., Xie X., Truong H., Nitschmann E., et al. Dietary conjugated linoleic acid decreases adipocyte size and favorably modifies adipokine status and insulin sensitivity in obese, insulin-resistant rats. Metabolism 2007, 56:1601-1611.
16. Chung S., Brown J.M., Provo J.N., Hopkins R., McIntosh M.K. Conjugated linoleic acid promotes human adipocyte insulin resistance through NFkappaB-dependent cytokine production. J Biol Chem 2005, 280:38445-38456.
17. Kennedy A., Overman A., Lapoint K., Hopkins R., West T., Chuang C.C., et al. Conjugated linoleic acid-mediated inflammation and insulin resistance in human adipocytes are attenuated by resveratrol. J Lipid Res 2009, 50:225-232.
18. Tsuboyama-Kasaoka N., Takahashi M., Tanemura K., Kim H.J., Tange T., Okuyama H., et al. Conjugated linoleic acid supplementation reduces adipose tissue by apoptosis and develops lipodystrophy in mice. Diabetes 2000, 49:1534-1542.
19. Halade G.V., Rahman M.M., Fernandes G. Differential effects of conjugated linoleic acid isomers in insulin-resistant female C57Bl/6J mice. J Nutr Biochem 2010, 21:332-337.
20. Kelley D.S., Vemuri M., Adkins Y., Gill S.H., Fedor D., Mackey B.E. Flaxseed oil prevents trans-10, cis-12-conjugated linoleic acid-induced insulin resistance in mice. Br J Nutr 2009, 101:701-708.
21. Hommelberg P.P., Langen R.C., Schols A.M., van Essen A.L., Snepvangers F.J., Mensink R.P., et al. Trans fatty acid-induced NF-kappaB activation does not induce insulin resistance in cultured murine skeletal muscle cells. Lipids 2010, 45:285-290.
22. Ross S.A., Gulve E.A., Wang M. Chemistry and biochemistry of Type 2 diabetes. Chem Rev 2004, 104:1255-1282.
23. Kasuga M., Karlsson F.A., Kahn C.R. Insulin stimulates the phosphorylation of the 95,000-dalton subunit of its own receptor. Science 1982, 215:185-187.
24. Despres J.P., Marette A. Obesity and insulin resistance. Epidemiologic, metabolic and molecular aspects. Contemp Endocrinol 1999, 1:51-82.
25. Zaid H., Antonescu C.N., Randhawa V.K., Klip A. Insulin action on glucose transporters through molecular switches, tracks and tethers. Biochem J 2008, 413:201-215.
26. Peck G.R., Chavez J.A., Roach W.G., Budnik B.A., Lane W.S., Karlsson H.K., et al. Insulin-stimulated phosphorylation of the Rab GTPase-activating protein TBC1D1 regulates GLUT4 translocation. J Biol Chem 2009, 284:30016-30023.
27. Steinberg G.R., Kemp B.E. AMPK in health and disease. Physiol Rev 2009, 89:1025-1078.
28. Woods A., Johnstone S.R., Dickerson K., Leiper F.C., Fryer L.G., Neumann D., et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 2003, 13:2004-2008.
29. Lizcano J.M., Goransson O., Toth R., Deak M., Morrice N.A., Boudeau J., et al. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J 2004, 23:833-843.
30. Buhl E.S., Jessen N., Schmitz O., Pedersen S.B., Pedersen O., Holman G.D., et al. Chronic treatment with 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside increases insulin-stimulated glucose uptake and GLUT4 translocation in rat skeletal muscles in a fiber type-specific manner. Diabetes 2001, 50:12-17.
31. Kramer H.F., Witczak C.A., Fujii N., Jessen N., Taylor E.B., Arnolds D.E., et al. Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes 2006, 55:2067-2076.
32. Schmidt J., Liebscher K., Merten N., Grundmann M., Mielenz M., Sauerwein H., et al. Conjugated linoleic acids mediate insulin release through islet G protein-coupled receptor FFA1/GPR40. J Biol Chem 2011, 286:11890-11894.
33. Brown J.M., Boysen M.S., Chung S., Fabiyi O., Morrison R.F., Mandrup S., et al. Conjugated linoleic acid induces human adipocyte delipidation: autocrine/paracrine regulation of MEK/ERK signaling by adipocytokines. J Biol Chem 2004, 279:26735-26747.
34. Kennedy A., Martinez K., Chung S., LaPoint K., Hopkins R., Schmidt S.F., et al. Inflammation and insulin resistance induced by trans-10, cis-12 conjugated linoleic acid depend on intracellular calcium levels in primary cultures of human adipocytes. J Lipid Res 2010, 51:1906-1917.
35. Hsu Y.C., Meng X., Ou L., Ip M.M. Activation of the AMP-activated protein kinase-p38 MAP kinase pathway mediates apoptosis induced by conjugated linoleic acid in p53-mutant mouse mammary tumor cells. Cell Signal 2010, 22:590-599.
36. Lauritzen H.P., Galbo H., Brandauer J., Goodyear L.J., Ploug T. Large GLUT4 vesicles are stationary while locally and reversibly depleted during transient insulin stimulation of skeletal muscle of living mice: imaging analysis of GLUT4-enhanced green fluorescent protein vesicle dynamics. Diabetes 2008, 57:315-324.
37. Mu J., Brozinick J.T., Valladares O., Bucan M., Birnbaum M.J. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 2001, 7:1085-1094.
38. Yau L., Litchie B., Zahradka P. MIBG, an inhibitor of arginine-dependent mono(ADP-ribosyl)ation, prevents differentiation of L6 skeletal myoblasts by inhibiting expression of myogenin and p21(cip1). Exp Cell Res 2004, 301:320-330.
39. Hommelberg P.P., Plat J., Langen R.C., Schols A.M., Mensink R.P. Fatty acid-induced NF-kappaB activation and insulin resistance in skeletal muscle are chain length dependent. Am J Physiol Endocrinol Metab 2009, 296:E114-120.
40. Zahradka P., Yau L., Lalonde C., Buchko J., Thomas S., Werner J., et al. Modulation of the vascular smooth muscle angiotensin subtype 2 (AT2) receptor by angiotensin II. Biochem Biophys Res Commun 1998, 252:476-480.
41. Yamashita R., Saito T., Satoh S., Aoki K., Kaburagi Y., Sekihara H. Effects of dehydroepiandrosterone on gluconeogenic enzymes and glucose uptake in human hepatoma cell line, HepG2. Endocr J 2005, 52:727-733.
42. Rasband W.S. ImageJ 1997-2010, U.S. National Institutes of Health, Bethesda (Md). 1.43 ed.
43. Yau L., Zahradka P. PGE(2) stimulates vascular smooth muscle cell proliferation via the EP2 receptor. Mol Cell Endocrinol 2003, 203:77-90.
44. Yamada K., Saito M., Matsuoka H., Inagaki N. A real-time method of imaging glucose uptake in single, living mammalian cells. Nat Protoc 2007, 2:753-762.
45. Satory D.L., Smith S.B. Conjugated linoleic acid inhibits proliferation but stimulates lipid filling of murine 3T3-L1 preadipocytes. J Nutr 1999, 129:92-97.
46. Evans M., Geigerman C., Cook J., Curtis L., Kuebler B., McIntosh M. Conjugated linoleic acid suppresses triglyceride accumulation and induces apoptosis in 3T3-L1 preadipocytes. Lipids 2000, 35:899-910.
47. Ebstensen R.D., Plagemann P.G. Cytochalasin B: inhibition of glucose and glucosamine transport. Proc Natl Acad Sci U S A 1972, 69:1430-1434.
48. Fazakerley D.J., Holman G.D., Marley A., James D.E., Stockli J., Coster A.C. Kinetic evidence for unique regulation of GLUT4 trafficking by insulin and AMP-activated protein kinase activators in L6 myotubes. J Biol Chem 2010, 285:1653-1660.
49. Kramer H.F., Witczak C.A., Taylor E.B., Fujii N., Hirshman M.F., Goodyear L.J. AS160 regulates insulin- and contraction-stimulated glucose uptake in mouse skeletal muscle. J Biol Chem 2006, 281:31478-31485.
50. Arcaro A., Aubert M., Espinosa del Hierro M.E., Khanzada U.K., Angelidou S., Tetley T.D., et al. Critical role for lipid raft-associated Src kinases in activation of PI3K-Akt signalling. Cell Signal 2007, 19:1081-1092.
51. Alkhateeb H., Chabowski A., Glatz J.F., Gurd B., Luiken J.J., Bonen A. Restoring As160 phosphorylation rescues skeletal muscle insulin resistance and fatty acid oxidation while not reducing intramuscular lipids. Am J Physiol Endocrinol Metab 2009, 297:E1056-E1066.
52. Bruss M.D., Arias E.B., Lienhard G.E., Cartee G.D. Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes 2005, 54:41-50.
53. Treebak J.T., Glund S., Deshmukh A., Klein D.K., Long Y.C., Jensen T.E., et al. AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits. Diabetes 2006, 55:2051-2058.
54. Merrill G.F., Kurth E.J., Hardie D.G., Winder W.W. AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol 1997, 273:E1107-E1112.
55. Qin H., Liu Y., Lu N., Li Y., Sun C.H. cis-9,trans-11-Conjugated linoleic acid activates AMP-activated protein kinase in attenuation of insulin resistance in C2C12 myotubes. J Agric Food Chem 2009, 57:4452-4458.
56. Long Y.C., Cheng Z., Copps K.D., White M.F. Insulin receptor substrates Irs1 and Irs2 coordinate skeletal muscle growth and metabolism via the Akt and AMPK pathways. Mol Cell Biol 2011, 31:430-441.
57. Yang J., Holman G.D. Insulin and contraction stimulate exocytosis, but increased AMP-activated protein kinase activity resulting from oxidative metabolism stress slows endocytosis of GLUT4 in cardiomyocytes. J Biol Chem 2005, 280:4070-4078.
58. Berggren J.R., Tanner C.J., Koves T.R., Muoio D.M., Houmard J.A. Glucose uptake in muscle cell cultures from endurance-trained men. Med Sci Sports Exerc 2005, 37:579-584.