Gestational protein restriction impairs insulin regulated glucose transport mechanisms in gastrocnemius muscles of adult male offspring

Endocrinology

Volumn 155, Issue 8, 2014, Pages 3036-3046

  Blesson, Chellakkan S ^a   Sathishkumar, Kunju ^b   Chinnathambi, Vijayakumar ^b   Yallampalli, Chandrasekhar ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; DIET, PROTEIN-RESTRICTED; FEMALE; GLUCOSE; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORTER TYPE 4; GTPASE-ACTIVATING PROTEINS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; MALE; MUSCLE, SKELETAL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RECEPTOR, INSULIN; WEIGHT GAIN;

EID: 84904989278     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1094     Document Type: Article

References (52)

1. DeFronzo RA. Insulin resistance, lipotoxicity, type 2 diabetes and atherosclerosis: the missing links. The Claude Bernard Lecture2009. Diabetologia. 2010; 53:1270-1287.
2. Moller DE, Kaufman KD. Metabolic syndrome: a clinical and molecular perspective. Annu Rev Med. 2005; 56:45-62.
3. Martin-Gronert MS, Ozanne SE. Metabolic programming of insulin action and secretion. Diabetes Obes Metab. 2012; 14(SUPPL. 3):29-39.
4. Stocker CJ, Arch JR, Cawthorne MA. Fetal origins of insulin resistance and obesity. Proc Nutr Soc. 2005; 64:143-151.
5. Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007; 261:412-417.
6. Ozanne SE, Olsen GS, Hansen LL, et al. Early growth restriction leads to down regulation of protein kinase Cζ and insulin resistance in skeletal muscle. J Endocrinol. 2003; 177:235-241.
7. Petry CJ, Dorling MW, Pawlak DB, Ozanne S.E., Hales CN. Diabetes in old male offspring of rat dams fed a reduced protein diet. IntJExp Diabetes Res. 2001; 2:139-143.
8. Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin M.S., Hales CN, Ozanne SE. Maternal protein restriction leads to hyperinsulin-emia and reduced insulin-signaling protein expression in 21-mo-old femaleratoffspring. Am J Physiol Regul Integr Comp Physiol. 2005; 288:R368-R373.
9. Zambrano E, Bautista CJ, Deas M, et al. A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006; 571(Pt 1):221-230.
10. Sugden MC, Holness MJ. Gender-specific programming of insulin secretion and action. J Endocrinol. 2002; 175:757-767.
11. Hales CN, Desai M, Ozanne SE, Crowther NJ. Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem Soc Trans. 1996; 24:341-350.
12. Aiken CE, Ozanne SE. Sex differences in developmental programming models. Reproduction. 2013; 145:R1-R13.
13. Abdul-Ghani MA, DeFronzo RA. Pathogenesis of insulin resistance in skeletal muscle. J Biomed Biotechnol. 2010; 2010:476279.
14. Choi K, Kim YB. Molecular mechanism of insulin resistance in obesity and type 2 diabetes. KoreanJ Intern Med. 2010; 25:119-129.
15. Gual P, Le Marchand-Brustel Y, Tanti JF. Positive and negative regulation of insulin signaling through IRS-1 phosphorylation. Biochimie. 2005; 87:99-109.
16. Klip A, Páquet MR. Glucose transport and glucose transporters in muscle and their metabolic regulation. Diabetes Care. 1990; 13: 228-243.
17. Ozanne SE, Wang CL, Coleman N, Smith GD. Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. Am J Physiol. 1996; 271:E1128-E1134.
18. Duque-Guimarães DE, Ozanne SE. Nutritional programming of insulin resistance: causes and consequences. Trends Endocrinol Metab. 2013; 24:525-535.
19. McArdle HJ, Andersen HS, Jones H, Gambling L. Fetal programming: causes and consequences as revealed by studies of dietary manipulation in rats-a review. Placenta. 2006; 27(suppl A):S56-S60.
20. Sathishkumar K, Balakrishnan M, Chinnathambi V, Gao H., Yallampalli C. Temporal alterations in vascular angiotensin receptors and vasomotor responses in offspring of protein-restricted rat dams. Am J Obstet Gynecol. 2012; 206:507.e501-507.e510.
21. Sathishkumar K, Elkins R, Yallampalli U, Yallampalli C. Protein restriction during pregnancy induces hypertension and impairs en-dothelium-dependent vascular function in adult female offspring. J Vasc Res. 2009; 46:229-239.
22. Sathishkumar K, Elkins R, Yallampalli U, Yallampalli C. Protein restriction during pregnancy induces hypertension in adult female rat offspring-influence of oestradiol. Br J Nutr. 2012; 107:665-673.
23. Aref AB, Ahmed OM, Ali LA, Semmler M. Maternal rat diabetes mellitus deleteriously affects insulin sensitivity and β-cell function in the offspring. J Diabetes Res. 2013; 2013:429154.
24. Gómez-Pérez Y, Gianotti M, Proenza AM, Lladó I. Age-related decline of skeletal muscle insulin sensitivity in rats: effect of sex and muscle type. Rejuvenation Res. 2011; 14:153-161.
25. Lai YC, Liu Y, Jacobs R, Rider MH. A novel PKB/Akt inhibitor, MK-2206, effectively inhibits insulin-stimulated glucose metabolism and protein synthesis in isolated rat skeletal muscle. Biochem J. 2012; 447:137-147.
26. Berends LM, Fernandez-Twinn DS, Martin-Gronert MS, Cripps R.L., Ozanne SE. Catch-up growth following intra-uterine growth-restriction programmes an insulin-resistant phenotype in adipose tissue. Int J Obes (Lond). 2013; 37:1051-1057.
27. Vo TX, Revesz A, Sohi G, Ma N., Hardy DB. Maternal protein restriction leads to enhanced hepatic gluconeogenic gene expression in adult male rat offspring due to impaired expression of the liver X receptor. J Endocrinol. 2013; 218:85-97.
28. Meyer MM, Levin K, Grimmsmann T, Beck-Nielsen H, Klein HH. Insulin signalling in skeletal muscle of subjects with or without type II-diabetes and first degree relatives of patients with the disease. Diabetologia. 2002; 45:813-822.
29. Sesti G, Federici M, Hribal ML, Lauro D, Sbraccia P., Lauro R. Defects of the insulin receptor substrate (IRS) system in human metabolic disorders. FASEB J. 2001; 15:2099-2111.
30. Youngren JF. Regulation of insulin receptor function. Cell Mol Life Sci. 2007; 64:873-891.
31. Gustafson TA, He W, Craparo A, Schaub C.D., O'Neill TJ. Phos-photyrosine-dependent interaction of SHC and insulin receptor substrate 1 with the NPEY motif of the insulin receptor via a novel non-SH2 domain. Mol Cell Biol. 1995; 15:2500-2508.
32. Boura-Halfon S, Zick Y. Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am J Physiol Endocrinol Metab. 2009; 296:E581-E591.
33. Timmers S, Schrauwen P, de Vogel J. Muscular diacylglycerol metabolism and insulin resistance. Physiol Behav. 2008; 94:242-251.
34. Glass DJ. PI3 kinase regulation of skeletal muscle hypertrophy and atrophy. Curr Top Microbiol Immunol. 2010; 346:267-278.
35. Copps KD, White MF. Regulation of insulin sensitivity by serine/ threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia. 2012; 55:2565-2582.
36. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson S.E., White MF. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem. 2002; 277:1531-1537.
37. Hennige AM, Stefan N, Kapp K., et al. Leptin down-regulates insulin action through phosphorylation of serine-318 in insulin receptor substrate 1. FASEB J. 2006; 20:1206-1208.
38. Yi Z, Langlais P, De Filippis EA, et al. Global assessment of regulation of phosphorylation of insulin receptor substrate-1 by insulin in vivo in human muscle. Diabetes. 2007; 56:1508-1516.
39. Weigert C, Kron M, Kalbacher H, et al. Interplay and effects of temporal changes in the phosphorylation state of serine-302, -307, and -318 of insulin receptor substrate-1 on insulin action in skeletal muscle cells. Mol Endocrinol. 2008; 22:2729-2740.
40. Copps KD, Hancer NJ, Opare-Ado L, Qiu W, Walsh C., White MF. Irs1 serine 307 promotes insulin sensitivity in mice. Cell Metab. 2010; 11:84-92.
41. Weigert C, Hennige AM, Brischmann T, et al. The phosphorylation of Ser318 of insulin receptor substrate 1 is not per se inhibitory in skeletal muscle cells but is necessary to trigger the attenuation of the insulin-stimulated signal. J Biol Chem. 2005; 280:37393-37399.
42. Weigert C, Hennige AM, Lehmann R, et al. Direct cross-talk of interleukin-6 and insulin signal transduction via insulin receptor substrate-1 in skeletal muscle cells. J Biol Chem. 2006; 281:7060-7067.
43. Bryant NJ, Govers R, James DE. Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol. 2002; 3:267-277.
44. Karlsson HK, Zierath JR, Kane S, Krook A., Lienhard GE, Wallberg-Henriksson H. Insulin-stimulated phosphorylation of the Akt substrate AS160 is impaired in skeletal muscle of type 2 diabetic subjects. Diabetes. 2005; 54:1692-1697.
45. Miinea CP, Sano H, Kane S, et al. AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem J. 2005; 391(Pt 1):87-93.
46. Lansey MN, Walker NN, Hargett SR, Stevens J.R., Keller SR. Deletion of Rab GAP AS160 modifies glucose uptake and GLUT4 translocation in primary skeletal muscles and adipocytes and impairs glucose homeostasis. Am J Physiol Endocrinol Metab. 2012; 303: E1273-E1286.
47. Eguez L, Lee A, Chavez JA, et al. Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein. Cell Metab. 2005; 2:263-272.
48. Zaid H, Antonescu CN, Randhawa VK, Klip A. Insulin action on glucose transporters through molecular switches, tracks and tethers. Biochem J. 2008; 413:201-215.
49. Larance M, Ramm G, Stöckli J, et al. Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J Biol Chem. 2005; 280:37803-37813.
50. Consitt LA, Van Meter J, Newton CA, et al. Impairments in site-specific AS160 phosphorylation and effects of exercise training. Diabetes. 2013; 62:3437-3447.
51. Funai K, Schweitzer GG, Sharma N, Kanzaki M, Cartee GD. Increased AS160phosphorylation, but not TBC1D1 phosphorylation, with increased postexercise insulin sensitivity in rat skeletal muscle. Am J Physiol Endocrinol Metab. 2009; 297:E242-E251.
52. Koumanov F, Holman GD. Thrifty Tbc1d1 and Tbc1d4 proteins link signalling and membrane trafficking pathways. Biochem J. 2007; 403:e9-e11.