Calorie restriction initiated at middle age improved glucose tolerance without affecting age-related impairments of insulin signaling in rat skeletal muscle

Experimental Gerontology

Volumn 41, Issue 9, 2006, Pages 837-845

  Park, Seongjoon ^a   Komatsu, Toshimitsu ^a   Hayashi, Hiroko ^a   Yamaza, Haruyoshi ^a   Chiba, Takuya ^a   Higami, Yoshikazu ^a   Kuramoto, Kazunao ^b   Shimokawa, Isao ^a  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

Author keywords

Aging; Calorie restriction; Glucose intolerance; Insulin resistance; Insulin signal; Skeletal muscle

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; INSULIN RECEPTOR; PROTEIN KINASE B; PROTEIN KINASE C; SODIUM CHLORIDE;

AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC RESTRICTION; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME IMMUNOASSAY; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; HORMONAL REGULATION; IMMUNOBLOTTING; INSULIN BLOOD LEVEL; INSULIN METABOLISM; INSULIN RESISTANCE; INSULIN RESPONSE; MALE; NONHUMAN; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ADIPOSE TISSUE; AGING; ANIMALS; BODY WEIGHT; CALORIC RESTRICTION; GLUCOSE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORTER TYPE 4; INSULIN; MALE; MEMBRANE PROTEINS; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, INBRED F344; SIGNAL TRANSDUCTION;

EID: 33749684748     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2006.06.055     Document Type: Article

References (43)

1. Ader M., Ni T.-C., and Bergman R.N. Importance of glucose per se to intravenous glucose tolerance: comparison of the minimal model prediction with direct measurements. Diabetes 34 (1985) 1092-1103
2. Bazotte R.B., Curi R., and Hell N.S. Metabolic changes caused by irregular-feeding schedule as compared with meal-feeding. Physiol. Behav. 46 (1989) 109-113
3. Bruning J.C., Michael M.D., Winnay J.N., Hayashi T., Horsch D., Accili D., Goodyear L.J., and Kahn C.R. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol. Cell. 2 (1998) 559-569
4. Cartee G.D., Kietzke E.W., and Briggs-Tung C. Adaptation of muscle glucose transport with caloric restriction in adult, middle-aged, and old rats. Am. J. Physiol. 266 (1994) R1443-R1447 (Regulatory Integrative Comp. Physiol. 35)
5. Dean D.J., Brozinick Jr. J.T., Cushman S.W., and Cartee G.D. Calorie restriction increases cell surface Glut-4 in insulin-stimulated skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 275 (1998) E957-E964
6. DeFronzo R.A., Jacot E., Jequier E., Maeder J., Wahren J., and Felber J.P. The effect of insulin in the disposal of intravenous glucose. Diabetes 30 (1981) 1000-1007
7. Duffy P.H., Feuers R.J., Leakey J.A., Nakamura K., Turturro A., and Hart R.W. Effect of chronic caloric restriction on physiological variables related to energy metabolism in the male Fischer 344 rat. Mech. Ageing Dev. 48 (1989) 117-1133
8. Egido E.M., Rodriguez-Gallardo J., Silvestre R.A., and Marco J. Inhibitory effect of ghrelin on insulin and pancreatic somatostatin secretion. Eur. J. Endocrinol. 146 (2002) 241-244
9. Gonzalez A.A., Kumar R., Mulligan J.D., Davis A.J., and Saupe K.W. Effects of aging on cardiac and skeletal muscle AMPK activity: basal activity, allosteric activation, and response to in vivo hypoxemia in mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 (2004) R1270-R1275
10. Henriksen E., Bourey R.E., Rodnick K.J., Koranyi M.A., Permutt M.A., and Holloszy J.O. Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. Am. J. Physiol. 259 (1990) E593-E598
11. Ishiki M., and Klip A. Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 146 (2005) 5071-5078
12. James D.E., Burleigh K.M., and Kraegen E.W. In vivo glucose metabolism in individual tissues of the rat. J. Biol. Chem. 261 (1986) 6366-6374
13. Jessen N., Pold R., Buhl E.S., Jensen L.S., Schmitz O., and Lund S. Effects of AICAR and exercise on insulin-stimulated glucose uptake, signaling, and GLUT-4 content in rat muscles. J. Appl. Physiol. 94 (2003) 1373-1379
14. Kalant N., Stewart J., and Kaplan R. Effect of diet restriction on glucose metabolism and insulin responsiveness in aging rats. Mech. Ageing Dev. 46 (1988) 89-104
15. Kim J.K., Michael M.D., Previs S.F., Peroni O.D., Mauvais-Jarvis F., Neschen S., Kahn B.B., Kahn C.R., and Shulman G.I. Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J. Clin. Invest. 105 (2000) 1791-1797
16. Konturek S.J., Pawlik W., Mysh W., Gustaw P., Sendur R., Mikos E., and Bielanski W. Comparison of organ uptake and disappearance half-time of human epidermal growth factor and insulin. Regul. Pept. 30 (1990) 137-148
17. Lane M.A., Ball S.S., Ingram D.K., Cutler R.G., Engel J., Read V., and Roth G.S. Diet restriction in rhesus monkeys lowers fasting and glucose-stimulated glucoregulatory end points. Am. J. Physiol. 268 (1995) E941-E948
18. Lang C.H. Rates and tissue sites of noninsulin- and insulin-mediated glucose uptake in diabetic rats. Proc. Soc. Exp. Biol. Med. 199 (1992) 81-87
19. Lim S.N., Bonzelius F., Low S.H., Wille H., Weimbs T., and Herman G.A. Identification of discrete classes of endosome-derived samll vesicles as a major cellular pool for recycling membrane proteins. Mol. Biol. Cell 12 (2001) 981-995
20. Longo V.D., and Finch C.E. Evolutionary medicine: from dwarf model systems to healthy centenarians?. Science 299 (2003) 1342-1346
21. Maheux P., Chen Y.D., Polonsky K.S., and Reaven G.M. Evidence that insulin can directly inhibit hepatic glucose production. Diabetologia 40 (1997) 1300-1306
22. Masoro E.J. Overview of caloric restriction and ageing. Mech. Ageing Develop. 126 (2005) 913-922
23. Masoro E.J., McCarter R.J., Katz M.S., and McMahan C.A. Dietary restriction alters characteristics of glucose fuel use. J. Gerontol. 47 (1992) B202-B208
24. McCarter R.J. Differential aging among skeletal muscles. In: Masoro, Edward J., Austad, and Steven N. (Eds). Handbook of the Biology of Aging. sixth ed. (2006), Academic Press, New York 470-497
25. McCarter R.J., and Palmer J. Energy metabolism and aging: a lifelong study of Fischer 344 rats. Am. J. Physiol. 263 (1992) E448-E452
26. McCurdy C.E., and Cartee G.D. Akt2 is essential for the full effect of calorie restriction on insulin-stimulated glucose uptake in skeletal muscle. Diabetes 54 (2005) 1349-1356
27. McCurdy C.E., Davidson R.T., and Cartee G.D. Brief calorie restriction increases Akt2 phosphorylation in insulin-stimulated rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 285 (2003) E693-E700
28. Meyer C.W., Korthaus D., Jagla W., Cornali E., Grosse J., Fuchs H., Klingenspor M., Roemheld S., Tschop M., Heldmaier G., De Angelis M.H., and Nehls M. Endocrinology 145 (2004) 2531-2541
29. Moltz J.H., and McDonald J.K. Neuropeptide Y: direct and indirect action on insulin secretion in the rat. Peptides 6 (1985) 1155-1159
30. Oliveira R.L., Ueno M., de Souza C.T., Pereira-da-Silva M., Gasparetti A.L., Bezzera R.M., Alberici L.C., Vercesi A.E., Saad M.J., and Velloso L.A. Cold-induced PGC-1alpha expression modulates muscle glucose uptake through an insulin receptor/Akt-independent, AMPK-dependent pathway. Am. J. Physiol. Endocrinol. Metab. 287 (2004) E686-E695
31. Park S.Y., Choi G.H., Choi H.I., Ryu J., Jung C.Y., and Lee W. Calorie restriction improves whole-body glucose disposal and insulin resistance in association with the increased adipocyte-specific GLUT4 expression in Otsuka Long-Evans Tokushima Fatty rats. Arch. Biochem. Biophys. 436 (2005) 276-284
32. Patel A.D., Stanley S.A., and Murphy K.G. Ghrelin stimulates insulin-induced glucose uptake in adipocytes. Regul. Pept. 134 (2005) 17-22
33. Reaven E., Wright D., Mondon C.E., Solomon R., Ho H., and Reaven G.M. Effect of age and diet on insulin secretion and insulin action in the rat. Diabetes 32 (1983) 175-180
34. Shimokawa I., Fukuyama T., Yanagihara-Outa K., Tomita M., Komatsu T., Higami Y., Tuchiya T., Chiba T., and Yamaza Y. Effects of caloric restriction on gene expression in the arcuate nucleus. Neurobiol. Aging 24 (2003) 117-123
35. Silvestre R.A., Egido E.M., Hernandez R., Leprince J., Chatenet D., Tollemer H., Chartrel N., Vaudry H., and Marco L. Urotensin-II is present in pancreatic extracts and inhibits insulin release in the perfused rat pancreas. Eur. J. Endocrinol. 151 (2004) 803-809
36. Toffolo, G.M., Basu, R., Dalla Man, C., Rizza, R.A., Cobelli, C., 2006. Assessment of postprandial glucose metabolism: conventional dual versus triple tracer method. Am. J. Physiol. Endocrinol. Metab. 23, in press, doi:10.1152/ajpendo.00461.2005.
37. Toshinai K., Mondal M.S., Nakazato M., Date Y., Murakami N., Kojima M., Kangawa K., and Matsukura S. Upregulation of ghrelin expression in the stomach upon fasting, insulin-induced hypoglycemia, and leptin administration. Biochem. Biophys. Res. Commun. 281 (2001) 1220-1225
38. Wetter T.J., Gazdag A.C., Dean D.J., and Cartee G.D. Effect of calorie restriction on in vivo glucose metabolism by individual tissues in rats. Am. J. Physiol. 276 (1999) E728-E738
39. Yamaza H., Komatsu T., Chiba T., Toyama H., To K., Higami Y., and Shimokawa I. A transgenic dwarf rat model as a tool for the study of calorie restriction and aging. Exp. Gerontol. 39 (2004) 269-272
40. Zheng D., MacLean P.S., Pohnert S.C., Knight J.B., Olson A.L., Winder W.W., and Dohm G.L. Regulation of muscle GLUT-4 transcription by AMP-activated protein kinase. J. Appl. Physiol. 91 (2001) 1073-1083
41. Zhu M., DeCabo R., Anson R.M., Ingram D.K., and Lane M.A. Caloric restriction modulates insulin receptor signaling in liver and skeletal muscle of rat. Nutrition 21 (2005) 378-388
42. Zhu M., Miura J., Lu L.X., Bernier M., DeCabo R., Lane M.A., Roth G.S., and Ingram D.K. Circulating adiponectin levels increase in rats on caloric restriction: the potential for insulin sensitization. Exp. Gerontol. 39 (2004) 1049-1059
43. Zisman A., Peroni O.D., Abel E.D., Michael M.D., Mauvais-Jarvis F., Lowell B.B., Wojtaszewski J.F., Hirshman M.F., Virkamaki A., Goodyear L.J., Kahn C.R., and Kahn B.B. Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat. Med. 6 (2000) 924-928