Nutrition
Volume 21, Issue 3 , Pages 378-388 , March 2005

Caloric restriction modulates insulin receptor signaling in liver and skeletal muscle of rat

  • Min Zhu, Ph.D.

      Affiliations

    • Laboratory of Experimental Gerontology, Gerontology Research Center, Intramural Research Program, National Institute on Aging, Baltimore, Maryland, USA
  • ,
  • Rafael de Cabo, Ph.D.

      Affiliations

    • Laboratory of Experimental Gerontology, Gerontology Research Center, Intramural Research Program, National Institute on Aging, Baltimore, Maryland, USA
  • ,
  • R. Michael Anson, Ph.D.

      Affiliations

    • Laboratory of Experimental Gerontology, Gerontology Research Center, Intramural Research Program, National Institute on Aging, Baltimore, Maryland, USA
  • ,
  • Donald K. Ingram, Ph.D.

      Affiliations

    • Laboratory of Experimental Gerontology, Gerontology Research Center, Intramural Research Program, National Institute on Aging, Baltimore, Maryland, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1-410-558-8180; fax: +1-410-558-8323.
  • ,
  • Mark A. Lane, Ph.D.

      Affiliations

    • Merck and Co., Inc., Rahway, New Jersey, USA

Received 17 February 2004 ,Accepted 23 June 2004.

References 

  1. Butler RN , Austad SN , Barzilai N , Braun A , Helfand S , Larsen PL , et al.   Longevity genes (from primitive organisms to humans) . J Gerontol A Biol Sci Med Sci . 2003;58:B581
  2. Kirkland JL . The biology of senescence (potential for prevention of disease) . Clin Geriatr Med . 2002;18:383–405
  3. Perls T , Kunkel LM , Puca AA . The genetics of exceptional human longevity . J Mol Neurosci . 2002;19:233–238
  4. Finch CE , Tanzi RE . Genetics of aging . Science . 1997;278:407–411
  5. Kimura KD , Tissenbaum HA , Liu Y , Ruvkun G . Daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans . Science . 1997;277:942–946
  6. Apfeld J , Kenyon C . Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span . Cell . 1998;95:199–210
  7. Kenyon C , Chang J , Gensch E , Rudner A , Tabtiang R . A C. elegans mutant that lives twice as long as wild type . Nature . 1993;366:461–464
  8. Larsen PL , Albert PS , Riddle DL . Genes that regulate both development and longevity in Caenorhabditis elegans . Genetics . 1995;139:1567–1583
  9. Tatar M , Kopelman A , Epstein D , Tu MP , Yin CM , Garofalo RS . A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function . Science . 2001;292:107–110
  10. Clancy DJ , Gems D , Harshman LG , Oldham S , Stocker H , Hafen E , et al.   Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein . Science . 2001;292:104–106
  11. Accili D , Drago J , Lee EJ , Johnson MD , Cool MH , Salvatore P , et al.   Early neonatal death in mice homozygous for a null allele of the insulin receptor gene . Nat Genet . 1996;12:106–109
  12. Wertheimer E , Lu SP , Backeljauw PF , Davenport ML , Taylor SI . Homozygous deletion of the human insulin receptor gene results in leprechaunism . Nat Genet . 1993;5:71–73
  13. Reaven GM . Pathophysiology of insulin resistance in human disease . Physiol Rev . 1995;75:473–486
  14. Kahn BB , Flier JS . Obesity and insulin resistance . J Clin Invest . 2000;106:473–481
  15. Matsuzawa Y , Funahashi T , Nakamura T . Molecular mechanism of metabolic syndrome X (contribution of adipocytokines adipocyte-derived bioactive substances) . Ann NY Acad Sci . 1999;18:146–154
  16. Bruning JC , Michael MD , Winnay JN , Hayashi T , Horsch D , Accili D , et al.   A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance . Mol Cell . 1998;2:559–569
  17. Kulkarni RN , Bruning JC , Winnay JN , Postic C , Magnuson MA , Kahn CR . Tissue-specific knockout of the insulin receptor in pancreatic beta cells creates an insulin secretory defect similar to that in type 2 diabetes . Cell . 1999;96:329–339
  18. Michael MD , Kulkarni RN , Postic C , Previs SF , Shulman GI , Magnuson MA , et al.   Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction . Mol Cell . 2000;6:87–97
  19. Bluher M , Michael MD , Peroni OD , Ueki K , Carter N , Kahn BB , et al.   Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance . Dev Cell . 2002;3:25–38
  20. Bluher M , Kahn BB , Kahn CR . Extended longevity in mice lacking the insulin receptor in adipose tissue . Science . 2003;299:572–574
  21. Roth GS , Ingram DK , Lane MA . Caloric restriction in primates and relevance to humans . Ann NY Acad Sci . 2001;928:305–315
  22. Weindruch R , Walford RL , Fligiel S , Guthrie D . The retardation of aging in mice by dietary restriction (longevity, cancer, immunity and lifetime energy intake) . J Nutr . 1986;116:641–654
  23. Masoro EJ . Caloric restriction and aging (an update) . Exp Gerontol . 2000;35:299–305
  24. McCay CM , Crowell MF , Maynard LA . The effect of retarded growth upon the length of life span and upon the ultimate body size. 1935 . Nutrition . 1989;5:155–172
  25. Saltiel AR , Kahn CR . Insulin signalling and the regulation of glucose and lipid metabolism . Nature . 2001;414:799–806
  26. Elchebly M , Payette P , Michaliszyn E , Cromlish W , Collins SA , Himms-Hagen J , et al.   Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene . Science . 1999;283:1544–1548
  27. Rondinone CM , Trevillyan JM , Clampit J , Gum RJ , Berg C , Kroeger P , et al.   Protein tyrosine phosphatase 1B reduction regulates adiposity and expression of genes involved in lipogenesis . Diabetes . 2002;51:2405–2411
  28. Zinker BA , Rondinone CM , Trevillyan JM , Gum RJ , Clampit JE , Waring JF , et al.   PTP1B antisense oligonucleotide lowers PTP1B protein, normalizes blood glucose, and improves insulin sensitivity in diabetic mice . Proc Natl Acad Sci USA . 2002;99:11357–11362
  29. Hribal ML , Oriente F , Accili D . Mouse models of insulin resistance . Am J Physiol Endocrinol Metab . 2002;282:E977–E981
  30. Muller-Wieland D , Streicher R , Siemeister G , Krone W . Molecular biology of insulin resistance . Exp Clin Endocrinol . 1993;101:17–29
  31. Baudry A , Leroux L , Jackerott M , Joshi RL . Genetic manipulation of insulin signaling, action and secretion in mice (insights into glucose homeostasis and pathogenesis of type 2 diabetes) . EMBO Rep . 2002;3:323–328
  32. Okauchi N , Mizuno A , Yoshimoto S , Zhu M , Sano T , Shima K . Is caloric restriction effective in preventing diabetes mellitus in the Otsuka Long Evans Tokushima fatty rat, a model of spontaneous non-insulin-dependent diabetes mellitus? . Diabetes Res Clin Pract . 1995;27:97–106
  33. Hansen BC , Bodkin NL . Primary prevention of diabetes mellitus by prevention of obesity in monkeys . Diabetes . 1993;42:1809–1814
  34. Youngren JF , Paik J , Barnard RJ . Impaired insulin-receptor autophosphorylation is an early defect in fat-fed, insulin-resistant rats . J Appl Physiol . 2001;91:2240–2247
  35. Friedman JE , Ishizuka T , Liu S , Farrell CJ , Bedol D , Koletsky RJ , et al.   Reduced insulin receptor signaling in the obese spontaneously hypertensive Koletsky rat . Am J Physiol . 1997;273:E1014–E1023
  36. Pender C , Ortmeyer HK , Hansen BC , Goldfine ID , Youngren JF . Elevated plasma cell membrane glycoprotein levels and diminished insulin receptor autophosphorylation in obese, insulin-resistant rhesus monkeys . Metabolism . 2002;51:465–470
  37. Gulve EA , Henriksen EJ , Rodnick KJ , Youn JH , Holloszy JO . Glucose transporters and glucose transport in skeletal muscles of 1-to 25-mo-old rats . Am J Physiol . 1993;264:E319–E327
  38. Liu F , Chernoff J . Protein tyrosine phosphatase 1B interacts with and is tyrosine phosphorylated by the epidermal growth factor receptor . Biochem J . 1997;327:139–145
  39. Egawa K , Maegawa H , Shimizu S , Morino K , Nishio Y , Bryer-Ash M , et al.   Protein-tyrosine phosphatase-1B negatively regulates insulin signaling in l6 myocytes and Fao hepatoma cells . J Biol Chem . 2001;276:10207–10211
  40. Byon JC , Kusari AB , Kusari J . Protein-tyrosine phosphatase-1B acts as a negative regulator of insulin signal transduction . Mol Cell Biochem . 1998;182:101–108
  41. Klaman LD , Boss O , Peroni OD , Kim JK , Martino JL , Zabolotny JM , et al.   Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice . Mol Cell Biol . 2000;20:5479–5489
  42. Kennedy BP , Ramachandran C . Protein tyrosine phosphatase-1B in diabetes . Biochem Pharmacol . 2000;60:877–883
  43. Nadiv O , Shinitzky M , Manu H , Hecht D , Roberts CT , LeRoith D , et al.   Elevated protein tyrosine phosphatase activity and increased membrane viscosity are associated with impaired activation of the insulin receptor kinase in old rats . Biochem J . 1994;298:443–450
  44. Dreyfuss G , Hentze M , Lamond AI . From transcript to protein . Cell . 1996;85:963–972
  45. Jacobson A , Peltz SW . Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells . Annu Rev Biochem . 1996;65:693–739
  46. Combs TP , Wagner JA , Berger J , Doebber T , Wang WJ , Zhang BB , et al.   Induction of adipocyte complement-related protein of 30 kilodaltons by PPARgamma agonists (a potential mechanism of insulin sensitization) . Endocrinology . 2002;143:998–1007
  47. Hotta K , Funahashi T , Bodkin NL , Ortmeyer HK , Arita Y , Hansen BC , et al.   Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys . Diabetes . 2001;50:1126–1133
  48. Lindsay RS , Funahashi T , Hanson RL , Matsuzawa Y , Tanaka S , Tataranni PA , et al.   Adiponectin and development of type 2 diabetes in the Pima Indian population . Lancet . 2002;360:57–58
  49. Stefan N , Vozarova B , Funahashi T , Matsuzawa Y , Weyer C , Lindsay RS , et al.   Plasma adiponectin concentration is associated with skeletal muscle insulin receptor tyrosine phosphorylation, and low plasma concentration precedes a decrease in whole-body insulin sensitivity in humans . Diabetes . 2002;51:1884–1888
  50. Berg AH , Combs TP , Du X , Brownlee M , Scherer PE . The adipocyte-secreted protein Acrp30 enhances hepatic insulin action . Nat Med . 2001;7:947–953
  51. Yamauchi T , Kamon J , Waki H , Terauchi Y , Kubota N , Hara K , et al.   The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity . Nat Med . 2001;7:941–946
  52. Fruebis J , Tsao TS , Javorschi S , Ebbets-Reed D , Erickson MR , Yen FT , et al.   Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice . Proc Natl Acad Sci USA . 2001;98:2005–2010
  53. Combs TP , Berg AH , Obici S , Scherer PE , Rossetti L . Endogenous glucose production is inhibited by the adipose-derived protein Acrp30 . J Clin Invest . 2001;108:1875–1881
  54. Kersten S , Desvergne B , Wahli W . Roles of PPARs in health and disease . Nature . 2000;405:421–424
  55. Ye JM , Iglesias MA , Watson DG , Ellis B , Wood L , Jensen PB , et al.   PPARalpha/gamma ragaglitazar eliminates fatty liver and enhances insulin action in fat-fed rats in the absence of hepatomegaly . Am J Physiol Endocrinol Metab . 2003;284:E531–E540
  56. Madison LL , Uger RH , Rencz K . The physiologic significance of secretion of insulin into portal circulation: II. Effect of rate of administration of glucagon-free insulin on magnitude of peripheral and hepatic actions . Metabolism . 1960;9:97–108
  57. Elahi D , Muller DC , Egan JM , Andres R , Veldhuist J , Meneilly GS . Glucose tolerance, glucose utilization and insulin secretion in ageing . Novartis Found Symp . 2002;242:242–246
  58. Chang AM , Halter JB . Aging and insulin secretion . Am J Physiol Endocrinol Metab . 2003;284:E7–E12

PII: S0899-9007(04)00299-0

doi: 10.1016/j.nut.2004.06.030

Nutrition
Volume 21, Issue 3 , Pages 378-388 , March 2005