Ingestion of carbohydrate-rich supplements during gestation programs insulin and leptin resistance but not body weight gain in adult rat offspring

Frontiers in Physiology

Volumn 3 JUN, Issue , 2012, Pages

  Beck, Bernard ^a   Richy, Sébastien ^a   Archer, Zoe A ^b   Mercer, Julian G ^b  

^a UNIVERSITÉ DE LORRAINE   (France)

^b ROWETT RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Adipose tissue distribution; Dietary preference; Fetal programming; Ghrelin; High fat; Hypothalamic Ob Rb expression

Indexed keywords

EID: 84866393230     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00224     Document Type: Article

References (61)

1. Ahren, B., Mansson, S., Gingerich, R. L., and Havel, P. J. (1997). Regulation of plasma leptin in mice: influence of age, high-fat diet, and fasting. Am. J. Physiol. 42, R113-R120.
2. Bayol, S. A., Farrington, S. J., and Stickland, N. C. (2007). A maternal "junk food" diet in pregnancy and lactation promotes an exacerbated taste for "junk food" and a greater propensity for obesity in rat offspring. Br. J. Nutr. 98, 843-851.
3. Beck, B. (2000). "Quantitative and macronutrient-related regulation of hypothalamic neuropeptide Y, galanin and neurotensin," in Neural and Metabolic Control of Macronu-trient Intake, eds H. R. Berthoud and R. J. Seeley (Boca Raton, FL: CRC Press), 455-464.
4. Beck, B. (2005). "The arcuate nucleus: its special place in the central networks that regulate feeding behavior," in Nutrient and Cell Signalling, ed. J. D. K. Zempleni (New-York: Dekker), 665-699.
5. Beck, B., and Richy, S. (2008). Differential long-term dietary regulation of adipokines, ghrelin, or cor-ticosterone: impact on adiposity. J. Endocrinol. 196,171-179.
6. Beck, B., Stricker-Krongrad, A., Burlet, A., Cumin, F., and Burlet, C. (2001). Plasma leptin and hypothalamic neuropeptide Y and galanin levels in Long-Evans rats with marked dietary preferences. Nutr. Neurosci. 4, 39-50.
7. Beck, B., Stricker-Krongrad, A., Burlet, A., Max, J. P., Musse, N., Nicolas, J. P., and Burlet, C. (1994). Macronutrient type independently of energy intake modulates hypothalamic neuropeptide Y in Long-Evans rats. Brain Res. Bull. 34,85-91.
8. Bispham, J., Gopalakrishnan, G. S., Dandrea, J., Wilson, V., Budge, H., Keisler, D. H., Broughton Pipkin, F., Stephenson, T., and Symonds, M. E. (2003). Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144, 3575-3585.
9. Bowen, D.J. (1992). Tasteandfoodpref-erence changes across the course of pregnancy. Appetite 19,233-242.
10. Brion, M. J. A., Ness, A. R., Rogers, I., Emmett, P., Cribb, V., Smith, G. D., and Lawlor, D. A. (2010). Maternal macronutrient and energy intakes in pregnancy and offspring intake at 10 y: exploring parental comparisons and prenatal effects. Am. J. Clin. Nutr. 91,748-756.
11. Buckley, A. J., Keseru, B., Briody, J., Thompson, M., Ozanne, S. E., and Thompson, C. H. (2005). Altered body composition and metabolism in the male offspring of high fat-fed rats. Metab. Clin. Exp. 54, 500-507.
12. Butte, N. F., Hopkinson, J. M., Mehta, N., Moon, J. K., and Smith, E. O. (1999). Adjustments in energy expenditure and substrate utilization during late pregnancy and lactation. Am. I Clin. Nutr. 69,299-307.
13. Butte, N. F., Wong, W W, Treuth, M. S., Ellis, K. J., and Smith, E. O. (2004). Energy requirements during pregnancy based on total energy expenditure and energy deposition. Am. J. Clin. Nutr. 79, 1078-1087.
14. Cerf, M. E., Chapman, C. S., Muller, C. J., and Louw, J. (2009). Gestational high-fat programming impairs insulin release and reduces Pdx-1 and glucokinase immunoreactivity in neonatal Wistar rats. Metab. Clin. Exp. 58, 1787-1792.
15. Chang, G. Q., Gaysinskaya, V., Karatayev, O., and Leibowitz, S. F. (2008). Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J. Neurosci. 28, 12107-12119.
16. Clegg, D. J., Benoit, S. C., Reed, J. A., Woods, S. C., DunnMeynell, A., and Levin, B. E. (2005). Reduced anorexic effects of insulin in obesity-prone rats fed a moderate-fat diet. Am. J. Physiol. 288, R981-R986.
17. Cnop, M., Landchild, M. J., Vidal, J., Havel, P. J., Knowles, N. G., Carr, D R., Wang, F., Hall, R. L., Boyko, E J., Retzlaff, B. M., Walden, C. E., Knopp,R. H.,andKahn,S. E. (2002). The concurrent accumulation of intra-abdominal and subcutaneous fat explains the association between insulin resistance and plasma leptin concentrations - distinct metabolic effects of two fat compartments. Diabetes 51,1005-1015.
18. Considine, R. V., Sinha, M. K., Heiman, M. L., Kriauciunas, A., Stephens, T. W., Nyce, M. R., Ohannesian, J. P., Marco, C. C., Mckee, L. J., Bauer, T. L., and Caro, J. F. (1996). Serum immunoreactive leptin concentrations in normal-weight and obese humans. N Engl. J. Med. 334, 292-295.
19. Cottrell, E. C., and Ozanne, S. E. (2008). Early life programming of obesity and metabolic disease. Physiol. Behav. 94, 17-28.
20. Despres, J. P. (2006). Is visceral obesity the cause of the metabolic syndrome? Ann. Med. 38, 52-63.
21. Dickens, G., and Trethowan, W. H. (1971). Cravings and aversions during pregnancy. J. Psychosom. Res. 15, 259-268.
22. Diouf, I., Charles, M. A., Ducimetiere, P., Basdevant, A., Eschwege, E., and Heude, B. (2010). Evolution of obesity prevalence in France. An age-period-cohort analysis. Epidemiology 21,360-365.
23. Dollet, J. M., Beck, B., Max, J. P., and Debry, G. (1987). Protein-energy malnutrition in pregnant rats improves adaptation of endocrine pancreas in malnourished offspring and induces insulin resistance after rehabilitation. Br. J. Nutr. 58, 415-425.
24. Dyrskog, S. E., Gregersen, S., and Her-mansen, K. (2005). High-fat feeding during gestation and nursing period have differential effects on the insulin secretory capacity in offspring from normal Wistar rats. Rev. Diabet. Stud. 2, 136-145.
25. FerezouViala, J., Roy, A. F., Serougne, C., Gripois, D., Parquet, M., Bailleux, V., Gertler, A., Delplanque, B., Djiane, J., Riottot, M., and Taouis, M. (2007). Long-term consequences of maternal high-fat feeding on hypothalamic leptin sensitivity and diet-induced obesity in the offspring. Am. J. Physiol. 293, R1056-R1062.
26. Fernandez Twinn, D. S., Wayman, A., Ekizoglou, S., Martin, M. S., Hales, C. N., and Ozanne, S. E. (2005). Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am. J. Physiol. 288, R368-R373.
27. Flegal, K. M., Carroll, M. D., Ogden, C. L., and Curtin, L. R. (2010). Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303, 235-241.
28. Godfrey, K. M., and Barker, D. J. P. (2000). Fetal nutrition and adult disease. Am. J. Clin. Nutr. 71, 1344S-1352S.
29. Gregersen, S., Dyrskog, S. E. U., Storlien, L. H., and Hermansen, K. (2005). Comparison of a high saturated fat diet with a high carbohydrate diet during pregnancy and lactation: effects on insulin sensitivity in offspring of rats. Metab. Clin. Exp. 54, 1316-1322.
30. Hausman, D. B., Mc Closkey, H. M., and Martin, R. J. (1991). Maternal fat type influences the growth and fatty acid composition of newborn and weanling rats.J. Nutr. 121, 1917-1923.
31. Hook,E. B. (1978). Dietary cravings and aversions during pregnancy. Am. J. Clin. Nutr. 31, 1355-1362.
32. Howie, G. J., Sloboda, D. M., Kamal, T., and Vickers, M. H. (2009). Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J. Physiol. (Lond.) 587,905-915.
33. Huang, X. F., Xin, X., McLennan, P., and Storlien, L. (2004). Role of fat amount and type in ameliorating diet-induced obesity: insights at the level of hypothalamic arcuate nucleus leptin receptor, neuropeptide Y and pro-opiomelanocortin mRNA expression. Diabetes Obes. Metab. 6, 35-44.
34. Irani, B. G., DunnMeynell, A. A., and Levin, B. E. (2007). Altered hypothalamic leptin, insulin, and melanocortin binding associated with moderate-fat diet and predisposition to obesity. Endocrinology 148,310-316.
35. James, P. (2004). Obesity: the worldwide epidemic. Clin. Dermatol. 22, 276-280.
36. Koski, K. G., and Hill, F. W. (1986). Effect of low carbohydrate diets during pregnancy on parturition and postnatal survival of the newborn rat pup. J. Nutr. 116, 1938-1948.
37. Koski, K. G., Hill, F. W., and Hurley, L. S. (1986). Effect of low carbohydrate diets during pregnancy on embryogenesis and fetal growth and development in rats. J. Nutr. 116, 1922-1937.
38. Kozak, R., Burlet, A., Burlet, C., and Beck, B. (2000). Dietary composition during fetal and neonatal life affects neuropeptide Y functioning in adult offspring. Brain Res. Dev. Brain Res. 125, 75-82.
39. Kozak, R., Mercer, J. G., Burlet, A., Moar, K.M.,Burlet,C.,andBeck,B. (1998). Hypothalamic neuropeptide Y content and mRNA expression in weanling rats subjected to dietary manipulations during fetal and neonatal life. Regul. Pept. 75, 397-402.
40. Kozak, R., Richy, S., and Beck, B. (2005). Persistent alterations in neuropeptide Y release in the paraventricular nucleus of rats subjected to dietary manipulation during early life. Eur. J. Neurosci. 21,2887-2892.
41. Leibowitz, S. F., Lucas, D. J., Leibowitz, K. L., and Jhanwar, Y. S. (1991). Developmental patterns of macronutrient intake in female and male rats from weaning to maturity. Physiol. Behav. 50,1167-1174.
42. Leturque, A., Ferre, P., Satabin, P., Kervran, A., and Girard, J. (1980). In vivo insulin resistance during pregnancy in the rat. Diabetologia 19,521-528.
43. Lin, S., Storlien, L. H., and Huang, X. F. (2000). Leptin receptor, NPY, POMC mRNA expression in the diet-induced obese mouse brain. Brain Res. 875, 89-95.
44. Manuel Apolinar, L., Zarate, A., Rocha, L., and Hernandez, M. (2010). Fetal malnutrition affects hypothalamic leptin receptor expression after birth in male mice. Arch. Med. Res. 41, 240-245.
45. Marlin, N. A. (1983). Early exposure to sugars influences the sugar preference of the adult rat. Physiol. Behav. 31,619-623.
46. Mercer, J. G., Hoggard, N., Williams, L. M., Lawrence, C. B., Hannah, L. T., and Trayhurn, P. (1996). Localization of leptin receptor mRNA and the long form splice variant (ob-rb) in mouse hypothala-mus and adjacent brain regions by in situ hybridization. FEBS Lett. 387, 113-116.
47. Morris, M. J., and Chen, H. (2009). Established maternal obesity in the rat reprograms hypothalamic appetite regulators and leptin signaling at birth. Int. J. Obes. 33, 115-122.
48. Moses, R. G., Shand, J. L., and Tapsell, L. C. (1997). The recurrence of gesta-tional diabetes: could dietary differences in fat intake be an explanation? Diabetes Care 20, 1647-1650.
49. Munzberg, H., Flier, J. S., and Bjorbaek, C. (2004). Region-specific leptin resistance within the hypothala-mus of diet-induced obese mice. Endocrinology 145, 4880-4889.
50. Nakashima, Y. (2008). Fish-oil high-fat diet intake of dams after day 5 of pregnancy and during lactation guards against excessive fat consumption of their weaning pups. J. Nutr. Sci. Vitaminol. 54, 46-53.
51. Page, K. C., Malik, R. E., Ripple, J. A., and Anday, E. K. (2009). Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to ahigh-fat diet in male offspring. Am. J. Physiol. 297, R1049-R1057.
52. Palou, M., Priego, T., Sanchez, J., Palou, A., and Pico, C. (2010). Sexual dimorphism in the lasting effects of moderate caloric restriction during gestation on energy homeosta-sis in rats is related with fetal programming of insulin and leptin resistance. Nutr. Metab. (Lond.) 7,69.
53. Phillips, D. I. W., Fall, C. H. D., Cooper, C., Norman, R. J., Robinson, J. S., and Owens, P. C. (1999). Size at birth and plasma leptin concentrations in adult life. Int. J. Obes. 23, 1025-1029.
54. Pope, J. F., Skinner, J. D., and Carruth, B. R. (1992). Cravings and aversions of pregnant adolescents. J. Am. Diet. Assoc. 92, 1479-1482.
55. Popkin, B. M. (2010). Recent dynamics suggest selected countries catching up to US obesity. Am. J. Clin. Nutr. 91,284S-288S.
56. Reed, J. A., Benoit, S. C., Pfluger, P. T., Tschoep, M. H., D'Alessio, D. A., and Seeley, R. J. (2008). Mice with chronically increased circulating ghrelin develop age-related glucose intolerance. Am.J. Physiol. 294, E752-E760.
57. Shiraev, T., Chen, H., and Morris, M. J. (2009). Differential effects of restricted versus unlimited high-fat feeding in rats on fat mass, plasma hormones and brain appetite regulators. J. Neuroendocrinol. 21, 602-609.
58. Srinivasan, M., Katewa, S. D., Palaniyap-pan, A., Pandya, J. D., and Patel, M. S. (2006). Maternal high-fat diet consumption results in fetal malpro-gramming predisposing to the onset of metabolic syndrome-like pheno-type in adulthood. Am. J. Physiol. 291,E792-E799.
59. Stricker-Krongrad, A., Cumin, F., Burlet, C., and Beck, B. (1998). Hypothalamic neuropeptide Y and plasma leptin after long-term high-fat feeding in the rat. Neurosci. Lett. 254, 157-160.
60. Warwick, Z. S., and Schiffman, S. S. (1992). Role of dietary fat in calorie intake and weight gain. Neurosci. Biobehav. Rev. 16,585-596.
61. Wu, Q., Mizushima, Y., Komiya, M., Matsuo, T., and Suzuki, M. (1998). Body fat accumulation in the male offspring of rats fed high-fat diet. J. Clin. Biochem. Nutr. 25, 71-79.