Time window-dependent effect of perinatal maternal protein restriction on insulin sensitivity and energy substrate oxidation in adult male offspring

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 307, Issue 2, 2014, Pages

  Agnoux, Aurore Martin ^a,b   Antignac, Jean Philippe ^c   Simard, Gilles ^d,e,f   Poupeau, Guillaume ^a,b   Darmaun, Dominique ^a,b   Parnet, Patricia ^a,b   Alexandre Gouabau, Marie Cécile ^a,b  

^a CEMAGREF   (France)

^b CRNH AUVERGNE   (France)

^c LUNAM UNIVERSITÉ   (France)

^d LUNAM Universite   (France)

^e INSERM   (France)

^f UNIVERSITÉ D'ANGERS   (France)

Author keywords

Energy metabolism; Insulin clamp; Metabolic programming; Perinatal nutrition; oxidation

Indexed keywords

AGING; ANIMALS; BLOOD GLUCOSE; DIET, PROTEIN-RESTRICTED; FEMALE; GLUCOSE CLAMP TECHNIQUE; INSULIN; INSULIN RESISTANCE; LACTATION; MITOCHONDRIA; OXIDATION-REDUCTION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84904287466     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00015.2014     Document Type: Article

References (83)

1. Adams SH, Hoppel CL, Lok KH, Zhao L, Wong SW, Minkler PE, Hwang DH, Newman JW, Garvey WT. Plasma acylcarnitine profiles suggest incomplete long-chain fatty acid β-oxidation and altered tricarboxylic acid cycle activity in type 2 diabetic African-American women. J Nutr 139: 1073-1081, 2009.
2. Albareda M, Rodriguez-Espinosa J, Murugo M, De Leiva A, Corcoy R. Assessment of insulin sensitivity and β-cell function from measurements in the fasting state and during an oral glucose tolerance test. Diabetologia 43: 1507-1511, 2000.
3. Alberti KG, Zimmet P, Shaw J. International Diabetes Federation: a consensus on Type 2 diabetes prevention. Diabet Med 24: 451-463, 2007.
4. Alexandre-Gouabau MC, Courant F, Le Gall G, Moyon T, Darmaun D, Parnet P, Coupe B, Antignac JP. Offspring metabolomic response to maternal protein restriction in a rat model of intrauterine growth restriction (IUGR). J Proteome Res 10: 3292-3302, 2011.
5. Bain JR, Stevens RD, Wenner BR, Ilkayeva O, Muoio DM, Newgard CB. Metabolomics applied to diabetes research: moving from information to knowledge. Diabetes 58: 2429-2443, 2009.
6. Boden G, Chen X. Effects of fatty acids and ketone bodies on basal insulin secretion in type 2 diabetes. Diabetes 48: 577-583, 1999.
7. Bremer AA, Mietus-Snyder M, Lustig RH. Toward a unifying hypothesis of metabolic syndrome. Pediatrics 129: 557-570, 2012.
8. Cacho J, Sevillano J, de Castro J, Herrera E, Ramos MDP. Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague-Dawley rats. Am J Physiol Endocrinol Metab 295: E1269-E1276, 2008.
9. Coupe B, Grit I, Hulin P, Randuineau G, Parnet P. Postnatal growth after intrauterine growth restriction alters central leptin signal and energy homeostasis. PLoS One 7: e30616, 2012.
10. Courant F, Pinel G, Bichon E, Monteau F, Antignac JP, Le Bizec B. Development of a metabolomic approach based on liquid chromatography-high resolution mass spectrometry to screen for clenbuterol abuse in calves. Analyst 134: 1637-1646, 2009.
11. Courant F, Royer AL, Chereau S, Morvan ML, Monteau F, Antignac JP, Le Bizec B. Implementation of a semi-automated strategy for the annotation of metabolomic fingerprints generated by liquid chromatography-high resolution mass spectrometry from biological samples. Analyst 137: 4958-4967, 2012.
12. Crandall DL, Fried SK, Francendese AA, Nickel M, DiGirolamo M. Lactate release from isolated rat adipocytes: influence of cell size, glucose concentration, insulin and epinephrine. Horm Metab Res 15: 326-329, 1983.
13. de Caestecker JS, Jazrawi RP, Nisbett JA, Joseph AE, Maxwell JD, Northfield TC. Direct assessment of the mechanism for a raised serum bile acid level in chronic liver disease. Eur J Gastroenterol Hepatol 7: 955-961, 1995.
14. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol Endocrinol Metab Gastrointest Physiol 237: E214-E223, 1979.
15. Desai M, Crowther NJ, Lucas A, Hales CN. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 76: 591-603, 1996.
16. Drynan L, Quant PA, Zammit VA. Flux control exerted by mitochondrial outer membrane carnitine palmitoyltransferase over β-oxidation, ketogenesis and tricarboxylic acid cycle activity in hepatocytes isolated from rats in different metabolic states. Biochem J 317: 791-795, 1996.
17. Eaton S. Control of mitochondrial β-oxidation flux. Prog Lipid Res 41: 197-239, 2002.
18. Fanca-Berthon P, Michel C, Pagniez A, Rival M, Van Seuningen I, Darmaun D, Hoebler C. Intrauterine growth restriction alters postnatal colonic barrier maturation in rats. Pediatr Res 66: 47-52, 2009.
19. Ferrannini E, Natali A, Camastra S, Nannipieri M, Mari A, Adam KP, Milburn MV, Kastenmüller G, Adamski J, Tuomi T. Early metabolic markers of the development of dysglycemia and type 2 diabetes and their physiological significance. Diabetes 62: 1730-1737, 2013.
20. Ferré P. The biology of peroxisome proliferator-activated receptors relationship with lipid metabolism and insulin sensitivity. Diabetes 53: S43-S50, 2004.
21. Fiehn O, Garvey WT, Newman JW, Lok KH, Hoppel CL, Adams SH. Plasma metabolomic profiles reflective of glucose homeostasis in nondiabetic and type 2 diabetic obese African-American women. PLoS One 5: e15234, 2010.
22. Floegel A, Stefan N, Yu Z, Muhlenbruch K, Drogan D, Joost HG, Fritsche A, Haring HU, Hrabe de Angelis M, Peters A, Roden M, Prehn C, Wang-Sattler R, Illig T, Schulze MB, Adamski J, Boeing H, Pischon T. Identification of serum metabolites associated with risk of type 2 diabetes using a targeted metabolomic approach. Diabetes 62: 639-648, 2013.
23. Gall WE, Beebe K, Lawton KA, Adam KP, Mitchell MW, Nakhle PJ, Ryals JA, Milburn MV, Nannipieri M, Camastra S. α-Hydroxybutyrate is an early biomarker of insulin resistance and glucose intolerance in a nondiabetic population. PLoS One 5: e10883, 2010.
24. Ganu R, Harris R, Collins K, Aagaard K. Maternal diet: a modulator for epigenomic regulation during development in nonhuman primates and humans. Int J Obes Suppl 2: S14-S18, 2012.
25. Gutt M, Davis CL, Spitzer SB, Llabre MM, Kumar M, Czarnecki EM, Schneiderman N, Skyler JS, Marks JB. Validation of the insulin sensitivity index [ISI (0,120)]: comparison with other measures. Diabetes Res Clin Pract 47: 177-184, 2000.
26. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD. Fetal and infant growth and impaired glucose tolerance at age 64. Br Med J 303: 1019-1022, 1991.
27. 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 24: 341-350, 1996.
28. Heim KE, Morrell JS, Ronan AM, Tagliaferro AR. Effects of ketamine-xylazine and isoflurane on insulin sensitivity in dehydroepiandrosterone sulfate-treated minipigs (Sus scrofa domestica). Comp Med 52: 233-237, 2002.
29. Herman MA, She P, Peroni OD, Lynch CJ, Kahn BB. Adipose tissue branched chain amino acid (BCAA) metabolism modulates circulating BCAA levels. J Biol Chem 285: 11348-11356, 2010.
30. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413: 179-183, 2001.
31. Kashyap S, Belfort R, Gastaldelli A, Pratipanawatr T, Berria R, Pratipanawatr W, Bajaj M, Mandarino L, DeFronzo R, Cusi K. A sustained increase in plasma free fatty acids impairs insulin secretion in nondiabetic subjects genetically predisposed to develop type 2 diabetes. Diabetes 52: 2461-2474, 2003.
32. Kelly G. Insulin resistance: lifestyle and nutritional interventions. Altern Med Rev: 5: 109-132, 2000.
33. Kobayashi M, Ikegami H, Fujisawa T, Nojima K, Kawabata Y, Noso S, Babaya N, Itoi-Babaya M, Yamaji K, Hiromine Y, Shibata M, Ogihara T. Prevention and treatment of obesity, insulin resistance, and diabetes by bile acid-binding resin. Diabetes 56: 239-247, 2007.
34. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7: 45-56, 2008.
35. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JRB, Newgard CB. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7: 45-56, 2008.
36. Krebs M, Brunmair B, Brehm A, Artwohl M, Szendroedi J, Nowotny P, Roth E, Fürnsinn C, Promintzer M, Anderwald C. The mammalian target of rapamycin pathway regulates nutrient-sensitive glucose uptake in man. Diabetes 56: 1600-1607, 2007.
37. Langley SC, Browne RF, Jackson AA. Altered glucose tolerance in rats exposed to maternal low protein diets in utero. Comp Biochem Physiol Physiol 109: 223-229, 1994.
38. Lefebvre P, Cariou B, Lien F, Kuipers F, Staels B. Role of bile acids and bile acid receptors in metabolic regulation. Physiol Rev 89: 147-191, 2009.
39. Liu Y, Dentin R, Chen D, Hedrick S, Ravnskjaer K, Schenk S, Milne J, Meyers DJ, Cole P, Yates J, 3rd Olefsky J, Guarente L, Montminy M. A fasting inducible switch modulates gluconeogenesis via activator/ coactivator exchange. Nature 456: 269-273, 2008.
40. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method. Methods 25: 402-408, 2001.
41. Lu J, Xie G, Jia W, Jia W. Insulin resistance and the metabolism of branched-chain amino acids. Front Med 7: 53-59, 2013.
42. Martin Agnoux A, Alexandre-Gouabau MC, Le Dréan G, Antignac JP, Parnet P. Relative contribution of foetal and post-natal nutritional periods on feeding regulation in adult rats. Acta Physiol (Oxf) 210: 188-201, 2014.
43. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412-419, 1985.
44. Mega C, Teixeira de Lemos E, Vala H, Fernandes R, Oliveira J, Mascarenhas-Melo F, Teixeira F, Reis F. Diabetic nephropathy amelioration by a low-dose sitagliptin in an animal model of type 2 diabetes (Zucker diabetic fatty rat). Exp Diabetes Res 2011: 162092, 2011.
45. Mihalik SJ, Goodpaster BH, Kelley DE, Chace DH, Vockley J, Toledo FG, DeLany JP. Increased levels of plasma acylcarnitines in obesity and type 2 diabetes and identification of a marker of glucolipotoxicity. Obesity (Silver Spring) 18: 1695-1700, 2010.
46. Mingorance C, Duluc L, Chalopin M, Simard G, Ducluzeau PH, Herrera MD, Alvarez de Sotomayor M, Andriantsitohaina R. Propionyl-L-carnitine corrects metabolic and cardiovascular alterations in dietinduced obese mice and improves liver respiratory chain activity. PLoS One 7: e34268, 2012.
47. Muniyappa R, Lee S, Chen H, Quon MJ. Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. Am J Physiol Endocrinol Metab 294: E15-E26, 2008.
48. Muoio DM, Newgard CB. Molecular and metabolic mechanisms of insulin resistance and β-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 9: 193-205, 2008.
49. Newgard CB. Interplay between lipids and branched-chain amino acids in development of insulin resistance. Cell Metab 15: 606-614, 2012.
50. Nonogaki K. New insights into sympathetic regulation of glucose and fat metabolism. Diabetologia 43: 533-549, 2000.
51. Orozco-Solis R, Matos RJ, Lopes de Souza S, Grit I, Kaeffer B, Manhaes de Castro R, Bolanos-Jimenez F. Perinatal nutrient restriction induces long-lasting alterations in the circadian expression pattern of genes regulating food intake and energy metabolism. Int J Obes (Lond) 35: 990-1000, 2011.
52. Ozanne SE, Hales CN. Early programming of glucose-insulin metabolism. Trends Endocrinol Metab 13: 368-373, 2002.
53. Ozanne SE, Wang CL, Coleman N, Smith GD. Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. Am J Physiol Endocrinol Metab 271: E1128-E1134, 1996.
54. Passos MC, da Fonte Ramos C, Dutra SC, Mouco T, de Moura EG. Long-term effects of malnutrition during lactation on the thyroid function of offspring. Horm Metab Res 34: 40-43, 2002.
55. Petry CJ, Dorling MW, Pawlak DB, Ozanne SE, Hales CN. Diabetes in old male offspring of rat dams fed a reduced protein diet. Int J Exp Diabetes Res 2: 139-143, 2001.
56. Puigserver P, Rhee J, Donovan J, Walkey CJ, Yoon JC, Oriente F, Kitamura Y, Altomonte J, Dong H, Accili D, Spiegelman BM. Insulinregulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature 423: 550-555, 2003.
57. Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1: 785-789, 1963.
58. Ridderstrale M, Groop L. Genetic dissection of type 2 diabetes. Mol Cell Endocrinol 297: 10-17, 2009.
59. Rossetti L, Giaccari A. Relative contribution of glycogen synthesis and glycolysis to insulin-mediated glucose uptake. A dose-response euglycemic clamp study in normal and diabetic rats. J Clin Invest 85: 1785, 1990.
60. Rueda-Clausen CF, Dolinsky VW, Morton JS, Proctor SD, Dyck JR, Davidge ST. Hypoxia-induced intrauterine growth restriction increases the susceptibility of rats to high-fat diet-induced metabolic syndrome. Diabetes 60: 507-516, 2011.
61. Saccenti E, Hoefsloot HC, Smilde AK, Westerhuis JA, Hendriks MM. Reflections on univariate and multivariate analysis of metabolomics data. Metabolomics 1-14, 2013.
62. Salek RM, Maguire ML, Bentley E, Rubtsov DV, Hough T, Cheeseman M, Nunez D, Sweatman BC, Haselden JN, Cox RD, Connor SC, Griffin JL. A metabolomic comparison of urinary changes in type 2 diabetes in mouse, rat, and human. Physiol Genomics 29: 99-108, 2007.
63. Schooneman MG, Vaz FM, Houten SM, Soeters MR. Acylcarnitines: reflecting or inflicting insulin resistance? Diabetes 62: 1-8, 2013.
64. Snoeck A, Remacle C, Reusens B, Hoet JJ. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57: 107-118, 1990.
65. Soeters MR, Serlie MJ, Sauerwein HP, Duran M, Ruiter JP, Kulik W, Ackermans MTT, Minkler PE, Hoppel CL, Wanders RJ. Characterization of D-3-hydroxybutyrylcarnitine (ketocarnitine): an identified ketosisinduced metabolite. Metabolism 61: 966-973, 2012.
66. Stefan N, Stumvoll M, Bogardus C, Tataranni PA. Elevated plasma nonesterified fatty acids are associated with deterioration of acute insulin response in IGT but not NGT. Am J Physiol Endocrinol Metab 284: E1156-E1161, 2003.
67. Stocker CJ, Wargent ET, Martin-Gronert MS, Cripps RL, O'Dowd JF, Zaibi MS, Cottrell EC, Mercer JG, Duncan JS, Cawthorne MA, Ozanne SE, Arch JR. Leanness in postnatally nutritionally programmed rats is associated with increased sensitivity to leptin and a melanocortin receptor agonist and decreased sensitivity to neuropeptide Y. Int J Obes (Lond) 36: 1040-1046, 2012.
68. Stoffers DA, Desai BM, DeLeon DD, Simmons RA. Neonatal exendin-4 prevents the development of diabetes in the intrauterine growth retarded rat. Diabetes 52: 734-740, 2003.
69. Storlien L, Oakes ND, Kelley DE. Metabolic flexibility. Proc Nutr Soc 63: 363-368, 2004.
70. Su X, Han X, Mancuso DJ, Abendschein DR, Gross RW. Accumulation of long-chain acylcarnitine and 3-hydroxy acylcarnitine molecular species in diabetic myocardium: identification of alterations in mitochondrial fatty acid processing in diabetic myocardium by shotgun lipidomics. Biochemistry 44: 5234-5245, 2005.
71. Tan B, Li X, Yin Y, Wu Z, Liu C, Tekwe CD, Wu G. Regulatory roles for L-arginine in reducing white adipose tissue. Front Biosci 17: 2237-2246, 2012.
72. Theys N, Ahn MT, Bouckenooghe T, Reusens B, Remacle C. Maternal malnutrition programs pancreatic islet mitochondrial dysfunction in the adult offspring. J Nutr Biochem 22: 985-994, 2011.
73. Tran TT, Gupta N, Goh T, Naigamwalla D, Chia MC, Koohestani N, Mehrotra S, McKeown-Eyssen G, Giacca A, Bruce WR. Direct measure of insulin sensitivity with the hyperinsulinemic-euglycemic clamp and surrogate measures of insulin sensitivity with the oral glucose tolerance test correlations with aberrant crypt foci promotion in rats. Cancer Epidemiol Biomarkers Prev 12: 47-56, 2003.
74. Tran TT, Kahn CR. Transplantation of adipose tissue and stem cells: role in metabolism and disease. Nat Rev Endocrinol 6: 195-213, 2010.
75. Unger RH. Lipotoxic diseases. Annu Rev Med 53: 319-336, 2002.
76. van Loon LJ, Saris WH, Verhagen H, Wagenmakers AJ. Plasma insulin responses after ingestion of different amino acid or protein mixtures with carbohydrate. Am J Clin Nutr 72: 96-105, 2000.
77. 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 218: 85-97, 2013.
78. Wakil SJ, and Abu-Elheiga LA. Fatty acid metabolism: target for metabolic syndrome. J Lipid Res 50 Suppl: S138-S143, 2009.
79. Wallace T, Matthews D. The assessment of insulin resistance in man. Diabet Med 19: 527-534, 2002.
80. Wang-Sattler R, Yu Z, Herder C, Messias AC, Floegel A, He Y, Heim K, Campillos M, Holzapfel C, Thorand B, Grallert H, Xu T, Bader E, Huth C, Mittelstrass K, Doring A, Meisinger C, Gieger C, Prehn C, Roemisch-Margl W, Carstensen M, Xie L, Yamanaka-Okumura H, Xing G, Ceglarek U, Thiery J, Giani G, Lickert H, Lin X, Li Y, Boeing H, Joost HG, de Angelis MH, Rathmann W, Suhre K, Prokisch H, Peters A, Meitinger T, Roden M, Wichmann HE, Pischon T, Adamski J, Illig T. Novel biomarkers for pre-diabetes identified by metabolomics. Mol Syst Biol 8: 615, 2012.
81. White MF. IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab 283: E413-E422, 2002.
82. Zambrano E, Bautista CJ, Deas M, Martinez-Samayoa PM, Gonzalez-Zamorano M, Ledesma H, Morales J, Larrea F, Nathanielsz PW. 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 571: 221-230, 2006.
83. 2 in male rats. Physiol Res 59: 973-978, 2010.