Preventing the calorie restriction-induced increase in insulin-stimulated Akt2 phosphorylation eliminates calorie restriction's effect on glucose uptake in skeletal muscle

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 11, 2012, Pages 1735-1740

  Sharma, Naveen ^a   Arias, Edward B ^a   Sequea, Donel A ^b   Cartee, Gregory D ^a,b,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Caloric restriction; Glucose transport; GLUT4; Insulin resistance; Insulin sensitivity

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; DEOXYGLUCOSE; FILAMIN C; INSULIN; INSULIN RECEPTOR; PROTEIN KINASE B BETA; PROTEIN KINASE B INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALORIC RESTRICTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; GLUCOSE TRANSPORT; INSULIN RESISTANCE; INSULIN SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SKELETAL MUSCLE;

ANIMALS; CALORIC RESTRICTION; CONTRACTILE PROTEINS; GLUCOSE; HETEROCYCLIC COMPOUNDS, 3-RING; INSULIN; MICROFILAMENT PROTEINS; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTOR, INSULIN;

MUS; RATTUS;

EID: 84865077987     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.07.012     Document Type: Article

References (41)

1. Omodei D., Fontana L. Calorie restriction and prevention of age-associated chronic disease. FEBS Lett. 2011, 585:1537-1542.
2. Dolinsky V.W., Dyck J.R. Calorie restriction and resveratrol in cardiovascular health and disease. Biochim. Biophys. Acta 2011, 1812:1477-1489.
3. Gazdag A.C., Dumke C.L., Kahn C.R., Cartee G.D. Calorie restriction increases insulin-stimulated glucose transport in skeletal muscle from IRS-1 knockout mice. Diabetes 1999, 48:1930-1936.
4. Masoro E.J. Caloric restriction-induced life extension of rats and mice: a critique of proposed mechanisms. Biochim. Biophys. Acta 2009, 1790:1040-1048.
5. Gupta G., She L., Ma X.H., Yang X.M., Hu M., Cases J.A., Vuguin P., Rossetti L., Barzilai N. Aging does not contribute to the decline in insulin action on storage of muscle glycogen in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000, 278:R111-R117.
6. Kemnitz J.W., Roecker E.B., Weindruch R., Elson D.F., Baum S.T., Bergman R.N. Dietary restriction increases insulin sensitivity and lowers blood glucose in rhesus monkeys. Am. J. Physiol. 1994, 266:E540-E547.
7. Kemnitz J.W. Calorie restriction and aging in nonhuman primates. ILAR J. 2011, 52:66-77.
8. Fontana L., Partridge L., Longo V.D. Extending healthy life span-from yeast to humans. Science 2010, 328:321-326.
9. Anderson R.M., Weindruch R. The caloric restriction paradigm: implications for healthy human aging. Am. J. Hum. Biol. 2012, 24:101-106.
10. McCurdy C.E., Cartee G.D. Akt2 is essential for the full effect of calorie restriction on insulin-stimulated glucose uptake in skeletal muscle. Diabetes 2005, 54:1349-1356.
11. Sharma N., Arias E.B., Bhat A.D., Sequea D.A., Ho S., Croff K.K., Sajan M.P., Farese R.V., Cartee G.D. Mechanisms for increased insulin-stimulated Akt phosphorylation and glucose uptake in fast- and slow-twitch skeletal muscles of calorie-restricted rats. Am. J. Physiol. Endocrinol. Metab. 2011, 300:E966-E978.
12. Wetter T.J., Gazdag A.C., Dean D.J., Cartee G.D. Effect of calorie restriction on in vivo glucose metabolism by individual tissues in rats. Am. J. Physiol. 1999, 276:E728-E738.
13. Petersen K.F., Dufour S., Morino K., Yoo P.S., Cline G.W., Shulman G.I. Reversal of muscle insulin resistance by weight reduction in young, lean, insulin-resistant offspring of parents with type 2 diabetes. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(21):8236-8240.
14. Bae S.S., Cho H., Mu J., Birnbaum M.J. Isoform-specific regulation of insulin-dependent glucose uptake by Akt/protein kinase B. J. Biol. Chem. 2003, 278:49530-49536.
15. Hill M.M., Clark S.F., Tucker D.F., Birnbaum M.J., James D.E., Macaulay S.L. A role for protein kinase Bbeta/Akt2 in insulin-stimulated GLUT4 translocation in adipocytes. Mol. Cell. Biol. 1999, 19:7771-7781.
16. Katome T., Obata T., Matsushima R., Masuyama N., Cantley L.C., Gotoh Y., Kishi K., Shiota H., Ebina Y. Use of RNA interference-mediated gene silencing and adenoviral overexpression to elucidate the roles of AKT/protein kinase B isoforms in insulin actions. J. Biol. Chem. 2003, 278:28312-28323.
17. Ng Y., Ramm G., Lopez J.A., James D.E. Rapid activation of Akt2 is sufficient to stimulate GLUT4 translocation in 3T3-L1 adipocytes. Cell Metab. 2008, 7:348-356.
18. McCurdy C.E., Davidson R.T., Cartee G.D. Brief calorie restriction increases Akt2 phosphorylation in insulin-stimulated rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2003, 285:E693-E700.
19. Kane S., Sano H., Liu S.C., Asara J.M., Lane W.S., Garner C.C., Lienhard G.E. A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J. Biol. Chem. 2002, 277:22115-22118.
20. Gonzalez E., McGraw T.E. Insulin signaling diverges into Akt-dependent and -independent signals to regulate the recruitment/docking and the fusion of GLUT4 vesicles to the plasma membrane. Mol. Biol. Cell 2006, 17:4484-4493.
21. Kramer H.F., Witczak C.A., Fujii N., Jessen N., Taylor E.B., Arnolds D.E., Sakamoto K., Hirshman M.F., Goodyear L.J. Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes 2006, 55:2067-2076.
22. Tan S., Ng Y., James D.E. Next-generation Akt inhibitors provide greater specificity: effects on glucose metabolism in adipocytes. Biochem. J. 2011, 435:539-544.
23. Cherrin C., Haskell K., Howell B., Jones R., Leander K., Robinson R., Watkins A., Bilodeau M., Hoffman J., Sanderson P., Hartman G., Mahan E., Prueksaritanont T., Jiang G., She Q.B., Rosen N., Sepp-Lorenzino L., Defeo-Jones D., Huber H.E. An allosteric Akt inhibitor effectively blocks Akt signaling and tumor growth with only transient effects on glucose and insulin levels in vivo. Cancer Biol. Ther. 2010, 9:493-503.
24. Hirai H., Sootome H., Nakatsuru Y., Miyama K., Taguchi S., Tsujioka K., Ueno Y., Hatch H., Majumder P.K., Pan B.S., Kotani H. MK-2206, an allosteric Akt inhibitor, enhances antitumor efficacy by standard chemotherapeutic agents or molecular targeted drugs in vitro and in vivo. Mol. Cancer Ther. 2010, 9:1956-1967.
25. Yan L. MK-2206: a potent oral allosteric AKT inhibitor. AACR Annual Meeting 2009, Abstract Number: DDT01-01.
26. Cartee G.D., Bohn E.E. Growth hormone reduces glucose transport but not GLUT-1 or GLUT-4 in adult and old rats. Am. J. Physiol. 1995, 268:E902-E909.
27. Hansen P.A., Gulve E.A., Holloszy J.O. Suitability of 2-deoxyglucose for in vitro measurement of glucose transport activity in skeletal muscle. J. Appl. Physiol. 1994, 76:979-985.
28. Pal S.K., Reckamp K., Yu H., Figlin R.A. Akt inhibitors in clinical development for the treatment of cancer. Expert Opin. Investig. Drugs 2010, 19:1355-1366.
29. Yap T.A., Yan L., Patnaik A., Fearen I., Olmos D., Papadopoulos K., Baird R.D., Delgado L., Taylor A., Lupinacci L., Riisnaes R., Pope L.L., Heaton S.P., Thomas G., Garrett M.D., Sullivan D.M., de Bono J.S., Tolcher A.W. First-in-man clinical trial of the oral pan-AKT inhibitor MK-2206 in patients with advanced solid tumors. J. Clin. Oncol. 2011, 29:4688-4695.
30. Bilodeau M.T., Balitza A.E., Hoffman J.M., Manley P.J., Barnett S.F., Defeo-Jones D., Haskell K., Jones R.E., Leander K., Robinson R.G., Smith A.M., Huber H.E., Hartman G.D. Allosteric inhibitors of Akt1 and Akt2: a naphthyridinone with efficacy in an A2780 tumor xenograft model. Bioorg. Med. Chem. Lett. 2008, 18:3178-3182.
31. Kettle J.G., Brown S., Crafter C., Davies B.R., Dudley P., Fairley G., Faulder P., Fillery S., Greenwood H., Hawkins J., James M., Johnson K., Lane C.D., Pass M., Pink J.H., Plant H., Cosulich S.C. Diverse heterocyclic scaffolds as allosteric inhibitors of AKT. J. Med. Chem. 2012, 55:1261-1273.
32. Cheng Y., Zhang Y., Zhang L., Ren X., Huber-Keener K.J., Liu X., Zhou L., Liao J., Keihack H., Yan L., Rubin E., Yang J.M. MK-2206, a novel allosteric inhibitor of Akt, synergizes with gefitinib against malignant glioma via modulating both autophagy and apoptosis. Mol. Cancer Ther. 2012, 11:154-164.
33. Gonzalez E., McGraw T.E. The Akt kinases: isoform specificity in metabolism and cancer. Cell Cycle 2009, 8:2502-2508.
34. Murray J.T., Campbell D.G., Peggie M., Mora A., Cohen P. Identification of filamin C as a new physiological substrate of PKBalpha using KESTREL. Biochem. J. 2004, 384:489-494.
35. Fujita M., Mitsuhashi H., Isogai S., Nakata T., Kawakami A., Nonaka I., Noguchi S., Hayashi Y.K., Nishino I., Kudo A. Filamin C plays an essential role in the maintenance of the structural integrity of cardiac and skeletal muscles, revealed by the medaka mutant zacro. Dev. Biol. 2012, 361:79-89.
36. 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.
37. Ellis L., Clauser E., Morgan D.O., Edery M., Roth R.A., Rutter W.J. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell 1986, 45:721-732.
38. Bak J.F., Moller N., Schmitz O., Saaek A., Pedersen O. In vivo insulin action and muscle glycogen synthase activity in type 2 (non-insulin-dependent) diabetes mellitus: effects of diet treatment. Diabetologia 1992, 35:777-784.
39. Balage M., Grizard J., Manin M. Effect of calorie restriction on skeletal muscle and liver insulin binding in growing rat. Horm. Metab. Res. 1990, 22:207-214.
40. Cecchin F., Ittoop O., Sinha M.K., Caro J.F. Insulin resistance in uremia: insulin receptor kinase activity in liver and muscle from chronic uremic rats. Am. J. Physiol. 1988, 254:E394-E401.
41. Wang Z.Q., Bell-Farrow A.D., Sonntag W., Cefalu W.T. Effect of age and caloric restriction on insulin receptor binding and glucose transporter levels in aging rats. Exp. Gerontol. 1997, 32:671-684.