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Developmental programming of aging of isolated pancreatic islet glucose-stimulated insulin secretion in female offspring of mothers fed low-protein diets in pregnancy and/or lactation

Published online by Cambridge University Press:  10 July 2012

S. Morimoto ,
T. C. Sosa ,
L. Calzada ,
L. A. Reyes-Castro ,
E. Díaz-Díaz ,
A. Morales ,
P. W. Nathanielsz  and
E. Zambrano
S. Morimoto
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City, Mexico
T. C. Sosa
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City, Mexico
L. Calzada
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City, Mexico
L. A. Reyes-Castro
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City, Mexico
E. Díaz-Díaz
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City, Mexico
A. Morales
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City, Mexico
P. W. Nathanielsz
Affiliation:
Departament of Gynecology, Center for Pregnancy and Newborn Research, UTHSCSA, San Antonio Texas, USA
E. Zambrano*
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City, Mexico
*
*Address for correspondence: Dr. E. Zambrano, Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14000, Mexico. (Email [email protected])
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Abstract

Diabetes predisposition is determined by pancreatic islet insulin secretion and insulin resistance. We studied female rat offspring exposed to low-protein maternal diet (50% control protein diet) in pregnancy and/or lactation at postnatal days 36, 110 and 450. Rats were fed either control 20% casein diet (C) or restricted diet (R – 10% casein) during pregnancy. After delivery, mothers received either C or R diet until weaning to provide four offspring groups: CC, RR, CR and RC (first letter denoting maternal pregnancy diet and the second lactation diet). Serum glucose, insulin and homeostatic model assessment (HOMA) were measured. Pancreatic islets were isolated and in vitro insulin secretion quantified in low glucose (5 mM) and high glucose (11 mM). Serum glucose, insulin and HOMA were similar in all groups at 36 and 110 postnatal days. HOMA was only higher in RR at 450 postnatal days. Only CC demonstrated differences in glucose sensitivity of β-cells to high and low doses at the three ages studied. At 36 days, RR, CR and RC and at 450 days RR and RC groups did not show glucose-stimulated insulin secretion differences between low and high glucose. Aging-associated glucose-stimulated insulin secretion loss was affected by maternal dietary history, indicating that developmental programming must be considered a major factor in aging-related development of predisposition to later-life dysfunctional insulin metabolism. Female offspring islets’ insulin secretion was higher than previously reported in males.

Keywords

female ratHOMALangerhans isletslow-protein dietpancreas
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 3 , Issue 6 , December 2012 , pp. 483 - 488
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012 

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References

1.Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595–601.CrossRefGoogle ScholarPubMed
2.Carneiro, EM, Mello, MAR, Gobatto, CA, et al. Low protein diet impairs glucose-induced insulin secretion from and 45 Ca uptake by pancreatic rat islets. J Nutr Biochem. 1995; 6, 314–318.CrossRefGoogle Scholar
3.Choi, J, Li, C, McDonald, TJ, et al. Emergence of insulin resistance in juvenile baboon offspring of mothers exposed to moderate maternal nutrient reduction. Am J Physiol Regul Integr Comp Physiol. 2011; 301, R757–R762.CrossRefGoogle ScholarPubMed
4.Tarry-Adkins, JL, Ozanne, SE. Mechanisms of early life programming: current knowledge and future directions. Am J Clin Nutr. 2011; 94, 1765S–1771S.CrossRefGoogle ScholarPubMed
5.DeFronzo, RA. Glucose intolerance of aging. Diabetes Care. 1981; 4, 493–501.Google Scholar
6.Chang, AM, Halter, JB. Aging and insulin secretion. Am J Physiol Endocrinol Metab. 2003; 284, E7–E12.CrossRefGoogle ScholarPubMed
7.Morimoto, S, Calzada, L, Sosa, TC, et al. Emergence of ageing-related changes in insulin secretion by pancreatic islets of male rat offspring of mothers fed a low-protein diet. Br J Nutr. 2012; 107, 1562–1565.Google Scholar
8.Delghingaro-Augusto, V, Ferreira, F, Bordin, S, et al. A low protein diet alters gene expression in rat pancreatic islets. J Nutr. 2004; 134, 321–327.CrossRefGoogle ScholarPubMed
9.Siebel, AL, Mibus, A, De Blasio, MJ, et al. Improved lactational nutrition and postnatal growth ameliorates impairment of glucose tolerance by uteroplacental insufficiency in male rat offspring. Endocrinology. 2008; 149, 3067–3076.Google Scholar
10.Soriano, S, Gonzalez, A, Marroquí, L, et al. Reduced insulin secretion in protein malnourished mice is associated with multiple changes in the beta-cell stimulus-secretion coupling. Endocrinology. 2010; 151, 3543–3554.CrossRefGoogle ScholarPubMed
11.do Amaral, ME, Ueno, M, Oliveira, CA, et al. Reduced expression of SIRT1 is associated with diminished glucose-induced insulin secretion in islets from calorie-restricted rats. J Nutr Biochem. 2011; 22, 554–559.CrossRefGoogle ScholarPubMed
12.Zambrano, E, Rodriguez-Gonzalez, G, Guzman, C, et al. A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol. 2005; 563, 275–284.Google Scholar
13.Guzmán, C, Cabrera, R, Cárdenas, M, et al. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol. 2006; 572, 97–108.CrossRefGoogle ScholarPubMed
14.Cherif, H, Reusens, B, Ahn, MT, et al. Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. J Endocrinol. 1998; 159, 341–348.Google Scholar
15.Aguayo-Mazzucato, C, Sanchez-Soto, C, Godinez-Puig, V, et al. Restructuring of pancreatic islets and insulin secretion in a postnatal critical window. PLoS One. 2006; 1, e35.Google Scholar
16.Fernandez-Twinn, DS, Wayman, A, Ekizoglou, S, et al. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R368–R373.Google Scholar
17.Zambrano, E, Bautista, CJ, Deás, 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, 221–230.Google Scholar
18.Picarel-Blanchot, F, Alvarez, C, Bailbe, D, et al. Changes in insulin action and insulin secretion in the rat after dietary restriction early in life: influence of food restriction versus low-protein food restriction. Metabolism. 1995; 44, 1519–1526.Google Scholar
19.Chamson-Reig, A, Thyssen, SM, Hill, DJ, et al. Exposure of the pregnant rat to low protein diet causes impaired glucose homeostasis in the young adult offspring by different mechanisms in males and females. Exp Biol Med (Maywood). 2009; 234, 1425–1436.Google Scholar
20.Cherif, H, Reusens, B, Dahri, S, et al. A protein-restricted diet during pregnancy alters in vitro insulin secretion from islets of fetal Wistar rats. J Nutr. 2001; 131, 1555–1559.Google Scholar
21.Heywood, WE, Mian, N, Milla, PJ, et al. Programming of defective rat pancreatic beta-cell function in offspring from mothers fed a low-protein diet during gestation and the suckling periods. Clin Sci (Lond). 2004; 107, 37–45.CrossRefGoogle ScholarPubMed
22.Basu, R, Man, CD, Campioni, M, et al. Effects of age and sex on postprandial glucose metabolism differences in glucose turnover, insulin secretion, insulin action, and hepatic insulin extraction. Diabetes. 2006; 55, 2001–2014.CrossRefGoogle ScholarPubMed
23.Jensen, MD, Nielsen, S, Gupta, N, et al. Insulin clearance is different in men and women. Metabolism. 2012; 61, 525–530.Google Scholar
24.Basu, R, Breda, E, Oberg, AL, et al. Mechanisms of the age-associated deterioration in glucose tolerance: contribution of alterations in insulin secretion, action, and clearance. Diabetes. 2003; 52, 1738–1748.Google Scholar
25.Riant, E, Waget, A, Cogo, H, et al. Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology. 2010; 150, 2109–2117.Google Scholar
26.Louet, JF, LeMay, C, Mauvais-Jarvis, F. Antidiabetic actions of estrogen: insight from human and genetic mouse models. Curr Atheroscler Rep. 2004; 6, 180–185.CrossRefGoogle ScholarPubMed
27.Wong, WP, Tiano, JP, Liu, S, et al. Extranuclear estrogen receptor-alpha stimulates NeuroD1 binding to the insulin promoter and favors insulin synthesis. Proc Natl Acad Sci. 2010; 107, 13057–13062.Google Scholar
28.Ihm, SH, Moon, HJ, Kang, JG, et al. Effect of aging on insulin secretory function and expression of beta cell function-related genes of islets. Diabetes Res Clin Pract. 2007; 77, S150–S154.CrossRefGoogle ScholarPubMed
29.Wild, S, Roglic, G, Green, A, et al. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004; 27, 1047–1053.Google Scholar