Peroxisome proliferator-activated receptor-γ agonist improves skeletal muscle insulin signaling in the pregestational intrauterine growth-restricted rat offspring

American Journal of Physiology - Endocrinology and Metabolism

Volumn 297, Issue 2, 2009, Pages

  Oak, Shilpa ^a   Tran, Cang ^a   Castillo, Maria Olivia ^a   Thamotharan, Shanthie ^a   Thamotharan, Manikkavasagar ^a   Devaskar, Sherin U ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MDCC B2 375 ^*  (United States)

Author keywords

Fetal origins of adult disease; Glucose transporter; Metabolic programming; Protein kinase C

Indexed keywords

ADENOSINE PHOSPHATE; GLUCOSE TRANSPORTER 4; INSULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN P85; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE 1B; PROTEIN TYROSINE PHOSPHATASE 2; ROSIGLITAZONE; TENSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE; CHROMOSOME 10; CONTROLLED STUDY; DIET RESTRICTION; ENZYME ACTIVATION; FEMALE; GENE TRANSLOCATION; GESTATIONAL AGE; INTRAUTERINE GROWTH RETARDATION; NONHUMAN; NUTRIENT CONTENT; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; PROTEIN PHOSPHORYLATION; RAT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ALGORITHMS; ANIMALS; DRUG EVALUATION, PRECLINICAL; FEMALE; FETAL GROWTH RETARDATION; GLUCOSE TRANSPORTER TYPE 4; GROWTH; HYPOGLYCEMIC AGENTS; INSULIN; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; PPAR GAMMA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; SIGNAL TRANSDUCTION; THIAZOLIDINEDIONES;

EID: 68049101977     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00008.2009     Document Type: Article

References (57)

1. Aerts L, Holemans K, Van Assche FA. Maternal diabetes during pregnancy: consequences for the offspring. Diabetes Metab Rev 6: 147-167, 1990.
2. Aronoff S, Rosenblatt S, Braithwaite S, Egan JW, Mathisen AL, Schneider RL. Pioglitazone hydrochloride monotherapy improves glycemic control in the treatment of patients with type 2 diabetes: a 6-month randomized placebo-controlled dose-response study. The Pioglitazone 001 Study Group. Diabetes Care 23: 1605-1611, 2000.
3. Barker DJ. Fetal origins of coronary heart disease. Br Med J 311: 171-174, 1995.
4. Barker DJ, Osmond C, Forsen TJ, Kajantie E, Eriksson JG. Trajectories of growth among children who have coronary events as adults. N Engl J Med 353: 1802-1809, 2005.
5. Bhargava SK, Sachdev HS, Fall CH, Osmond C, Lakshmy R, Barker DJ, Biswas SK, Ramji S, Prabhakaran D, Reddy KS. Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthood. N Engl J Med 350: 865-875, 2004.
6. Boloker J, Gertz SJ, Simmons RA. Gestational diabetes leads to the development of diabetes in adulthood in the rat. Diabetes 51: 1499-1506, 2002.
7. Brunmair B, Gras F, Neschen S, Roden M, Wagner L, Waldhausi W, Furnsinn C. Direct thiazolidinedione action on isolated rat skeletal muscle fuel handling is independent of peroxisome proliferator-activated receptor-gamma mediated changes in gene expression. Diabetes 50: 2309-2315, 2001.
8. Burant CF, Sreenan S, Hirano K, Tai TA, Lohmiller J, Lukens J, Davidson NO, Ross S, Graves RA. Troglitazone action is independent of adipose tissue. J Clin Invest 100: 2900-2908, 1997.
9. Campbell IW. The clinical significance of PPAR gamma agonism. Curr Mol Med 5: 349-363, 2005.
10. Ceolotto G, Gallo A, Papparella I, Franco L, Murphy E, Iori E, Pagnin E, Fadini GP, Albiero M, Semplicini A, Avogaro A. Rosiglitazone reduces glucose-induced oxidative stress mediated by NAD(P)H oxidase via AMPK-dependent mechanism. Arterioscler Thromb Vasc Biol 27: 2627-2633, 2007.
11. Ching CK, Lai CK, Poon WT, Lui MC, Lam YH, Shek CC, Mak TW, Chan AY. Drug-induced hypoglycemia-new insight into an old problem. Hong Kong Med J 12: 334-338, 2006.
12. Cole HH, Hart GH. The effect of pregnancy and lactation on growth in the rat. Am J Physiol 123: 589-597, 1938.
13. Draelos MT, Jacobson AM, Weinger K, Widom B, Ryan CM, Finkelstein DM, Simpson DC. Cognitive function in patients with insulin-dependent diabetes mellitus during hyperglycemia and hypoglycemia. Am J Med 98: 135-144, 1995.
14. Eriksson JG, Osmond C, Kajantie E, Forsén TJ, Barker DJ. Patterns of growth among children who later develop type 2 diabetes or its risk factors. Diabetologia 49: 2853-2858, 2006.
15. Fecchi K, Volonte D, Hezel MP, Schmeck K, Galbiati F. Spatial and temporal regulation of GLUT4 translocation by flotillin-1 and caveolin-3 in skeletal muscle cells. FASEB J 20: 705-707, 2006.
16. Feig DS, Briggs GG, Koren G. Oral antidiabetic agents in pregnancy and lactation: a paradigm shift? Ann Pharmacother 41: 1174-1180, 2007.
17. Fritzius T, Frey AD, Schweneker M, Mayer D, Moelling K. WD-repeat-propeller-FYVE protein, ProF, binds VAMP2 and protein kinase C zeta. FEBS J 274: 1552-1566, 2007.
18. Garg M, Thamotharan M, Oak SA, Pan G, MacLaren DC, Lee PWN, Devaskar SU. Early exercise regimen improves insulin sensitivity in the intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 296: E272-E281, 2009.
19. Garg M, Thamotharan M, Rogers L, Bassilian S, Lee PWN, Devaskar SU. Glucose metabolic adaptations in the intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 290: E1218-E1226, 2006.
20. Goodyear LJ, Hirshman MF, Horton ES. Exercise-induced translocation of skeletal muscle glucose transporters. Am J Physiol Endocrinol Metab 261: E795-E799, 1991.
21. He J, Thamotharan M, Devaskar SU. Insulin-induced translocation of facilitative glucose transporters in fetal/neonatal rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 284: R1138-R1146, 2003.
22. Holemans K, Van Bree R, Verhaeghe J, Meurrens K, Van Assche FA. Maternal semistarvation and streptozotocin-diabetes in rats have different effects on the in-vivo glucose uptake by peripheral tissues in their female adult offspring. J Nutr 127: 1371-1376, 1997.
23. Holness MJ, Langdown ML, Sugden MC. Early-life programming of susceptibility to dysregulation of glucose metabolism and the development of Type 2 diabetes mellitus. Biochem J 349: 657-665, 2000.
24. Hovi P, Andersson S, Eriksson JG, Järvenpää AL, Strang-Karlsson S, Mäkitie O, Kajantie E. Glucose regulation in young adults with very low birth weight. N Engl J Med 356: 2053-2063, 2007.
25. Inzucchi SE, Maggs DG, Spollett GR, Page SL, Rife FS, Walton V, Shulman GI. Efficacy and metabolic effects of metformin and troglitazone in type II diabetes mellitus. N Engl J Med 338: 867-872, 1998.
26. Jensen CB, Martin-Gronert MS, Storgaard H, Madsbad S, Vaag A, Ozanne SE. Altered PI3-kinase/Akt signaling in skeletal muscle of young men with low birth weight. PLoS ONE 3: e3736, 2008.
27. Kanoh Y, Bandyopadhyay G, Sajan MP, Standaert ML, Farese RV. Rosiglitazone, insulin treatment and fasting correct defective activation of protein kinase C-zeta/lambda by insulin in vastus lateralis muscles and adipocytes of diabetic rats. Endocrinology 142: 1595-1605, 2001.
28. Kanoh Y, Bandyopadhyay G, Sajan MP, Standaert ML, Farese RV. Thiazolidinedione treatment enhances insulin effects on protein kinase C-zeta/lambda activation and glucose transport in adipocytes of nondiabetic and Goto-Kakizaki type II diabetic rats. J Biol Chem 275: 16690-16696, 2000.
29. Kersten S, Mandard S, Tan NS, Escher P, Metzger D, Chambon P, Gonzalez FJ, Desvergne B, Wahli W. Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J Biol Chem 275: 28488-28493, 2000.
30. Kurth-Kraczek DJ, Hirschman MF, Goodyear LJ, Winder WW. 5-AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48: 1667-1671, 1999.
31. Laudanna C, Mochly-Rosen D, Liron T, Constantin G, Butcher EC. Evidence of zeta protein kinase C involvement in polymorphonuclear neutrophil integrin-dependent adhesion and chemotaxis. J Biol Chem 273: 30306-30315, 1998.
32. Lessand SJ, Chen ZP, Watt MJ, Hashem M, Reid JJ, Febbraio MA, Kemp BE, Hawley JA. Chronic rosiglitazone treatment restores AMPK alpha2 activity in insulin-resistant rat skeletal muscle. Am J Physiol Endocrinol Metab 290: E251-E257, 2006.
33. Li P, Koike T, Qin B, Kubota M, Kawata Y, Jia YJ, Oshida Y. A high-fructose diet impairs Akt and PKCzeta phosphorylation and GLUT4 translocation in rat skeletal muscle. Horm Metab Res 40: 528-532, 2008.
34. Liu LZ, Zhao HL, Zuo J, Ho SK, Chan JC, Meng Y, Fang FD, Tong PC. Protein kinase Czeta mediates insulin-induced glucose transport through actin remodeling in L6 muscle cells. Mol Biol Cell 17: 2322-2330, 2006.
35. Loviscach M, Rehman N, Carter L, Mudaliar S, Mohadeen P, Ciaraldi TP, Veerkamp JH, Henry RR. Distribution of peroxisome proliferator-activated receptors (PPARs) in human skeletal muscle and adipose tissue: relation to insulin action. Diabetologia 43: 304-311, 2000.
36. Maroni P, Bendinelli P, Piccoletti R. Intracellular signal transduction pathways induced by leptin in C2C12 cells. Cell Biol Int 29: 542-550, 2005.
37. Miyazaki Y, He H, Mandarino LJ, De Fronzo RA. Rosiglitazone improves downstream insulin receptor signaling in type 2 diabetic patients. Diabetes 52: 1943-1950, 2003.
38. Oak SA, Tran C, Pan G, Thamotharan M, Devaskar SU. Perturbed skeletal muscle insulin signaling in the adult female intrauterine growth-restricted rat. Am J Physiol Endocrinol Metab 290: E1321-E1330, 2006.
39. Olefsky JM. Treatment of insulin resistance with peroxisome proliferator-activated receptor gamma agonists. J Clin Invest 106: 467-472, 2000.
40. Olefsky JM, Saltiel AR. PPARgamma and the treatment of insulin resistance. Trends Endocrinol Metab 11: 362-368, 2000.
41. Ozanne SE, Hales CN. Early programming of glucose-insulin metabolism. Trends Endocrinol Metab 13: 368-373, 2002.
42. Ozanne SE, Jensen CB, Tingey KJ, Storgaard H, Madsbad S, Vaag AA. Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia 48: 547-552, 2005.
43. Ozanne SE, Olsen GS, Hansen LL, Tingey KJ, Nave BT, Wang CL, Hartil K, Petry CJ, Buckley AJ, Mosthaf-Seedorf L. Early growth restriction leads to down regulation of protein kinase Czeta and insulin resistance in skeletal muscle. J Endocrinol 177: 235-241, 2003.
44. Phillips LS, Grunberger G, Miller E, Patwardhan R, Rappaport EB, Salzman A. Once- and twice-daily dosing with rosiglitazone improves glycemic control in patients with type 2 diabetes. Diabetes Care 24: 308-315, 2001.
45. Pinheiro AR, Salvucci ID, Aguila MB, Mandarim-de-Lacerda CA. Protein restriction during gestation and/or lactation causes adverse trans-generational effects on biometry and glucose metabolism in F1 and F2 progenies of rats. Clin Sci (Lond) 114: 381-392, 2008.
46. Rangwala SM, Lazar MA. Peroxisome proliferator-activated receptor gamma in diabetes and metabolism. Trends Pharmacol Sci 25: 331-336, 2004.
47. Reece EA, Hornko CJ. Prepregnancy care and the prevention of fetal malformations in the pregnancy complicated by diabetes. Clin Obstet Gynecol 50: 990-997, 2007.
48. Saltiel AR, Olefsky JM. Thiazolidinediones in the treatment of insulin resistance and type II diabetes. Diabetes 45: 1661-1669, 1996.
49. Scheen AJ. Thiazolidinediones and liver toxicity. Diabetes Metab 27: 305-313, 2001.
50. Sorensen HT, Thulstrup AM, Norgdard B, Engberg M, Madsen KM, Johnsen SP, Olsen J, Lauritzen T. Fetal growth and blood pressure in a Danish population aged 31-51 years. Scand Cardiovasc J 34: 390-395, 2000.
51. Starner CI, Schafer JA, Heaton AH, Gleason PP. Rosiglitazone and pioglitazone utilization from January 2007 through May 2008 associated with five risk-warning events. J Manag Care Pharm 14: 523-531, 2008.
52. Thamotharan M, Garg M, Oak S, Rogers LM, Pan G, Sangiorgi F, Lee PW, Devaskar SU. Transgenerational inheritance of the insulin-resistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 292: E1270-E1279, 2007.
53. Thamotharan M, Shin BC, Suddirikku DT, Thamotharan S, Garg M, Devaskar SU. Glut4 expression and subcellular localization in the intrauterine growth-restricted adult rat female offspring. Am J Physiol Endocrinol Metab 288: E935-E947, 2005.
54. Van Assche FA, Holemans K, Aerts L. Fetal growth and consequences of later life. J Perinat Med 26: 337-346, 1998.
55. Weinstein SP, Holand A, O'Boyle E, Habet RS. Effects of thiazolidinediones on glucocorticoid-induced insulin resistance and GLUT4 glucose transporter expression in rat skeletal muscle. Metabolism 42: 1365-1369, 1993.
56. Weyer C, Pratley RE, Lindsay RS, Tataranni PA. Relationship between birth weight and body composition, energy metabolism and sympathetic nervous system activity later in life. Obes Res 8: 559-565, 2000.
57. Zambrano E, Martinex-Samayoa PM, Bautista CJ, Deas M, Guillen L, Rodriquez-Gonzales GL, Guzman C, Larrea F, Nathanielsz PW. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol 566: 225-236, 2005.