Dietary protein deprivation upregulates insulin signaling and inhibits gluconeogenesis in rat liver

Journal of Molecular Endocrinology

Volumn 45, Issue 5, 2010, Pages 329-340

  Toyoshima, Yuka ^a,c   Tokita, Reiko ^c   Ohne, Yoichiro ^a   Hakuno, Fumihiko ^a   Noguchi, Tadashi ^b   Minami, Shiro ^c   Kato, Hisanori ^a,d   Takahashi, Shin Ichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b CHUBU UNIVERSITY   (Japan)

^c NIPPON MEDICAL SCHOOL   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (PYROPHOSPHATE);

ANALYTIC METHOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME SUBUNIT; GLUCONEOGENESIS; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; LIVER; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN RESTRICTION; PYRUVATE TOLERANCE TEST; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION;

ANIMALS; BLOOD GLUCOSE; DIET, PROTEIN-RESTRICTED; DIETARY PROTEINS; ENERGY METABOLISM; GLUCONEOGENESIS; HOMEOSTASIS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; LIVER; MALE; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTEIN DEFICIENCY; RATS; RATS, WISTAR; RECEPTOR, INSULIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UP-REGULATION;

EID: 78649550672     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-10-0102     Document Type: Article

References (39)

1. Agati JM, Yeagley D & Quinn PG 1998 Assessment of the roles of mitogen-activated protein kinase, phosphatidylinositol 3-kinase, protein kinase B, and protein kinase C in insulin inhibition of cAMP-induced phosphoenolpyruvate carboxykinase gene transcription. Journal of Biological Chemistry 273 18751-18759. (doi:10. 1074/jbc.273.30.18751)
2. Aparicio M, Chauveau P & Combe C 2001 Are supplemented lowprotein diets nutritionally safe? American Journal of Kidney Diseases 37 S71-S76. (doi:10.1053/ajkd.2001.20753)
3. Balage M, Grizard J, Sornet C, Simon J, Dardevet D & Manin M 1990 Insulin binding and receptor tyrosine kinase activity in rat liver and skeletal muscle: effect of starvation. Metabolism 39 366-373. (doi:10. 1016/0026-0495(90)90250-G) (Pubitemid 20146587)
4. Balmagiya T & Rozovski SJ 1983 Thermoregulation in young adult rats during short- and long-term protein malnutrition. Journal of Nutrition 113 228-238.
5. Barthel A & Schmoll D 2003 Novel concepts in insulin regulation of hepatic gluconeogenesis. American Journal of Physiology. Endocrinology and Metabolism 285 E685-E692. (doi:10.1152/ajpendo.00253.2003)
6. Bonkowski MS, Dominici FP, Arum O, Rocha JS, Al Regaiey KA, Westbrook R, Spong A, Panici J, Masternak MM, Kopchick JJ et al. 2009 Disruption of growth hormone receptor prevents calorie restriction from improving insulin action and longevity. PLoS ONE 4 e4567. (doi:10.1371/journal.pone.0004567)
7. Dean DJ & Cartee GD 2000 Calorie restriction increases insulinstimulated tyrosine phosphorylation of insulin receptor and insulin receptor substrate-1 in rat skeletal muscle. Acta Physiologica Scandinavica 169 133-139. (doi:10.1046/j.1365-201x.2000.00723.x)
8. DeFronzo RA, Soman V, Sherwin RS, Hendler R & Felig P 1978 Insulin binding to monocytes and insulin action in human obesity, starvation, and refeeding. Journal of Clinical Investigation 62 204-213. (doi:10.1172/JCI109108) (Pubitemid 8367354)
9. Endo Y, Fu Z, Abe K, Arai S & Kato H2002 Dietary protein quantity and quality affect rat hepatic gene expression. Journal of Nutrition 132 3632-3637.
10. Feinstein R, Kanety H, Papa MZ, Lunenfeld B & Karasik A 1993 Tumor necrosis factor-alpha suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. Journal of Biological Chemistry 268 26055-26058. (Pubitemid 2013440)
11. Garber AJ, Cryer PE, Santiago JV, Haymond MW, Pagliara AS & Kipnis DM 1976 The role of adrenergic mechanisms in the substrate and hormonal response to insulin-induced hypoglycemia in man. Journal of Clinical Investigation 58 7-15. (doi:10.1172/JCI108460)
12. Houde VP, Brule S, Festuccia WT, Blanchard PG, Bellmann K, Deshaies Y & Marette A 2010 Chronic rapamycin treatment causes glucose intolerance and hyperlipidemia by upregulating hepatic gluconeogenesis and impairing lipid deposition in adipose tissue. Diabetes 59 1338-1348. (doi:10.2337/db09-1324)
13. Kanety H, Feinstein R, Papa MZ, Hemi R & Karasik A 1995 Tumor necrosis factor alpha-induced phosphorylation of insulin receptor substrate-1 (IRS-1). Possible mechanism for suppression of insulin-stimulated tyrosine phosphorylation of IRS-1. Journal of Biological Chemistry 270 23780-23784. (doi:10.1074/jbc.270.40.23780)
14. Karasik A, Rothenberg PL, Yamada K, White MF & Kahn CR 1990 Increased protein kinase C activity is linked to reduced insulin receptor autophosphorylation in liver of starved rats. Journal of Biological Chemistry 265 10226-10231.
15. Kerouz NJ, Horsch D, Pons S & Kahn CR 1997 Differential regulation of insulin receptor substrates-1 and -2 (IRS-1 and IRS-2) and phosphatidylinositol 3-kinase isoforms in liver and muscle of the obese diabetic (ob/ob) mouse. Journal of Clinical Investigation 100 3164-3172. (doi:10.1172/JCI119872)
16. Kido Y, Burks DJ, Withers D, Bruning JC, Kahn CR, White MF & Accili D 2000 Tissue-specific insulin resistance in mice with mutations in the insulin receptor, IRS-1, and IRS-2. Journal of Clinical Investigation 105 199-205. (doi:10.1172/JCI7917) (Pubitemid 30054359)
17. Kubota N, Kubota T, Itoh S, Kumagai H, Kozono H, Takamoto I, Mineyama T, Ogata H, Tokuyama K, Ohsugi M et al. 2008 Dynamic functional relay between insulin receptor substrate 1 and 2 in hepatic insulin signaling during fasting and feeding. Cell Metabolism 8 49-64. (doi:10.1016/j.cmet.2008.05.007) (Pubitemid 351859226)
18. Miyake K, Ogawa W, Matsumoto M, Nakamura T, Sakaue H & Kasuga M 2002 Hyperinsulinemia, glucose intolerance, and dyslipidemia induced by acute inhibition of phosphoinositide 3-kinase signaling in the liver. Journal of Clinical Investigation 110 1483-1491. (doi:10.1172/JCI15880)
19. Nam TJ, Noguchi T, Funabiki R, Kato H, Miura Y & Naito H 1990 Correlation between the urinary excretion of acid-soluble peptides, fractional synthesis rate of whole body proteins, and plasma immunoreactive insulin-like growth factor-1/somatomedin C concentration in the rat. British Journal of Nutrition 63 515-520. (doi:10.1079/BJN19900138)
20. Obici S, Feng Z, Karkanias G, Baskin DG & Rossetti L 2002a Decreasing hypothalamic insulin receptors causes hyperphagia and insulin resistance in rats. Nature Neuroscience 5 566-572. (doi:10. 1038/nn0602-861) (Pubitemid 34568999)
21. Obici S, Zhang BB, Karkanias G & Rossetti L 2002b Hypothalamic insulin signaling is required for inhibition of glucose production. Nature Medicine 8 1376-1382. (doi:10.1038/nm798)
22. O'Brien RM & Granner DK 1996 Regulation of gene expression by insulin. Physiological Reviews 76 1109-1161.
23. Orban T, Landaker E, Ruan Z, Cordeman TP, Weitgasser R, Bonner- Weir S, Jackson RA & Patti ME 2001 High-fructose diet preserves beta-cell mass and prevents diabetes in nonobese diabetic mice: a potential role for increased insulin receptor substrate-2 expression. Metabolism 50 1369-1376. (doi:10.1053/meta.2001.27191)
24. Postic C, Dentin R & Girard J 2004 Role of the liver in the control of carbohydrate and lipid homeostasis. Diabetes & Metabolism 30 398-408. (doi:10.1016/S1262-3636(07)70133-7) (Pubitemid 39648006)
25. Previs SF, Withers DJ, Ren JM, White MF & Shulman GI 2000 Contrasting effects of IRS-1 versus IRS-2 gene disruption on carbohydrate and lipid metabolism in vivo. Journal of Biological Chemistry 275 38990-38994. (doi:10.1074/jbc.M006490200)
26. Reis MA, Carneiro EM, Mello MA, Boschero AC, Saad MJ & Velloso LA 1997 Glucose-induced insulin secretion is impaired and insulininduced phosphorylation of the insulin receptor and insulin receptor substrate-1 are increased in protein-deficient rats. Journal of Nutrition 127 403-410.
27. Rigalleau V, Aparicio M & Gin H 1998 Effects of low-protein diet on carbohydrate metabolism and energy expenditure. Journal of Renal Nutrition 8 175-178. (doi:10.1016/S1051-2276(98)90015-2)
28. Rojas FA, Hirata AE & Saad MJ 2001 Regulation of IRS-2 tyrosine phosphorylation in fasting and diabetes. Molecular and Cellular Endocrinology 183 63-69. (doi:10.1016/S0303-7207(01)00597-4)
29. Rui L, Aguirre V, Kim JK, Shulman GI, Lee A, Corbould A, Dunaif A & White MF 2001 Insulin/IGF-1 and TNF-alpha stimulate phosphorylation of IRS-1 at inhibitory Ser307 via distinct pathways. Journal of Clinical Investigation 107 181-189. (doi:10.1172/JCI10934)
30. Shimomura I, Matsuda M, Hammer RE, Bashmakov Y, Brown MS & Goldstein JL 2000 Decreased IRS-2 and increased SREBP-1c lead to mixed insulin resistance and sensitivity in livers of lipodystrophic and ob/ob mice. Molecular Cell 6 77-86. (doi:10.1016/S1097- 2765(00)00009-5)
31. Sykiotis GP & Papavassiliou AG 2001 Serine phosphorylation of insulin receptor substrate-1: a novel target for the reversal of insulin resistance. Molecular Endocrinology 15 1864-1869. (doi:10.1210/me. 15.11.1864)
32. Takahashi S, Kajikawa M, Umezawa T, Kato H, Miura Y, Nam TJ, Noguchi T & Naito H 1990 Effect of dietary proteins on the plasma immunoreactive insulin-like growth factor-1/somatomedin C concentration in the rat. British Journal of Nutrition 63 521-534. (doi:10.1079/BJN19900139)
33. Taniguchi CM, Ueki K & Kahn R 2005 Complementary roles of IRS-1 and IRS-2 in the hepatic regulation of metabolism. Journal of Clinical Investigation 115 718-727. (doi:10.1172/JCI23187) (Pubitemid 40322247)
34. Taniguchi CM, Emanuelli B & Kahn CR 2006 Critical nodes in signalling pathways: insights into insulin action. Nature Reviews. Molecular Cell Biology 7 85-96. (doi:10.1038/nrm1837)
35. Toyoshima Y, Ohne Y, Takahashi SI, Noguchi T & Kato H 2004 Dietary protein deprivation decreases the serine phosphorylation of insulin receptor substrate-1 in rat skeletal muscle. Journal of Molecular Endocrinology 32 519-531. (doi:10.1677/jme.0.0320519)
36. White MF 1998 The IRS-signalling system: a network of docking proteins that mediate insulin action. Molecular and Cellular Biochemistry 182 3-11. (doi:10.1023/A:1006806722619)
37. White MF 2002 IRS proteins and the common path to diabetes. American Journal of Physiology. Endocrinology and Metabolism 283 E413-E422. (doi:10.1152/ajpendo.00514.2001)
38. Wullschleger S, Loewith R & Hall MN 2006 TOR signaling in growth and metabolism. Cell 124 471-484. (doi:10.1016/j.cell.2006.01.016)
39. Zhu M, de Cabo R, Anson RM, Ingram DK & Lane MA 2005 Caloric restriction modulates insulin receptor signaling in liver and skeletal muscle of rat. Nutrition 21 378-388. (doi:10.1016/j.nut.2004.06.030) (Pubitemid 40387939)