Horm Metab Res 2009; 41(12): 866-873
DOI: 10.1055/s-0029-1233457
Animals, Clinical

© Georg Thieme Verlag KG Stuttgart · New York

Temporal Evaluation of Body Composition, Glucose Homeostasis and Lipid Profile of Male Rats Programmed by Maternal Protein Restriction During Lactation

A. T. S. Fagundes1 , E. G. Moura1 , M. C. F. Passos2 , A. P. Santos-Silva1 , E. de Oliveira1 , I. H. Trevenzoli1 , G. Casimiro-Lopes1 , J. F. Nogueira-Neto3 , P. C. Lisboa1
  • 1Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brasil
  • 2Departamento de Nutrição Aplicada, Instituto de Nutrição, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brasil
  • 3Laboratório de Lipídeos, Faculdade de Ciências Médicas, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brasil
Further Information

Publication History

received 13.01.2009

accepted 15.06.2009

Publication Date:
11 August 2009 (online)

Abstract

Neonatal protein restriction causes lower body weight and hormonal dysfunctions in 6 months-old rats. In this model, we studied the body composition, glycogen content, serum lipid, serum protein, and hormones related to glucose homeostasis in the offspring during development. At birth, lactating rats were divided into: control dams – fed a normal diet (23% protein) and protein restricted dams – fed a diet with 8% protein. After weaning, pups received normal diet. Offspring were killed at 21, 90, and 180 days-old. Protein restricted offspring showed lower visceral fat (90th day: 14%; 180th day: 19%) and lower total fat (90th day: 16%; 180th day: 14%) that explain their lower body weight. They presented lower glycemia (180th day: 17%), lower insulinemia (21st day: 63%; 180th day: 24%), higher adiponectinemia (21st day: 169%), higher liver glycogen (21st day: 104%), and higher muscle glycogen (180th day: 106%), suggesting a higher insulin sensitivity. The higher serum corticosterone (50%), higher adrenal total catecholamines content (98%) as well as in vitro catecholamine secretion (26%) of adult protein restricted offspring, suggest a programming stimulatory effect upon adrenal gland. They also presented several biochemical changes, such as lower serum total protein, albumin and globulin (21st day: 17, 21, 12%, respectively), higher LDL-c (21st day: 69%), lower triglycerides (21st day: 42%; 90th day: 39%), and lower total cholesterol (180th day: 16%). Thus, maternal protein restriction during lactation induces an energy-protein malnutrition, characterized by an impairment of the pup's protein anabolism and, after weaning, the lower adiposity suggests lower lipogenesis and higher lipolytic activity, probably caused by catecholamine and glucocorticoid action.

References

  • 1 Food and Agriculture Organization of the United Nations. .Undernourishment around the world. In: The state of food insecurity in the world 2004. Rome: FAO 2004: 6-17
  • 2 Barker DJ, Martyn CN, Osmond C, Hales CN, Fall CH. Growth in utero and serum cholesterol concentrations in adult life.  BMJ. 1993;  307 ((6918)) 1524-1527
  • 3 De Moura EG, Lisboa PC, Passos MC. Neonatal programming of neuroimmunomodulation – role of adipocytokines and neuropeptides.  Neuroimmunomodulation. 2008;  15 176-188
  • 4 Teixeira C, Passos M, Ramos C, Dutra S, Moura E. Leptin serum concentration in rats whose mothers were submitted to malnutrition during lactation.  J Nutr Biochem. 2002;  13 493-498
  • 5 De Moura EG, Lisboa PC, Custódio CM, Nunes MT, De Picoli Souza K, Passos MC. Malnutrition during lactation changes growth hormone mRNA expression in the offspring at weaning and at adulthood.  J Nutr Biochem. 2007;  18 134-139
  • 6 Lisboa PC, Fagundes AT, Denolato AT, Oliveira E, Bonomo IT, Alves SB, Curty FH, Passos MC, Moura EG. Neonatal low-protein diet changes deiodinase activities and pituitary TSH response to TRH in adult rats.  Exp Biol Med (Maywood). 2008;  233 57-63
  • 7 Fagundes AT, Moura EG, Passos MC, Oliveira E, Toste FP, Bonomo IT, Trevenzoli IH, Garcia RM, Lisboa PC. Maternal low protein diet during lactation programmes the body composition and the glucose homeostasis in the adult rat offspring.  Br J Nutr. 2007;  98 922-928
  • 8 Bayne K. Revised guide for the care and use of laboratory animals available. American Physiological Society.  Physiologist. 1996;  39 208-211
  • 9 Reeves PG, Nielsen FH, Fahey GC. AIN-93 Purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76 rodent diet.  J Nutr. 1993;  123 1939-1951
  • 10 Lowry OH, Rosebrough NJ, Farr AL, Randall R. Protein measurement with the Folin phenol reagent.  J Biol Chem. 1951;  193 265-275
  • 11 Casimiro-Lopes G, Alves SB, Salerno VP, Passos MCF, Lisboa PC, Moura EG. Maximum acute exercise tolerance in hyperthyroid and hypothyroid rats subjected to forced swimming.  Horm Metab Res. 2008;  40 276-280
  • 12 Trevenzoli IH, Valle MMR, Machado FB, Garcia RMG, Passos MCF, Lisboa PC, Moura EG. Neonatal hyperleptinemia programmes adrenal medullary function in adult rats: effects on cardiovascular parameters.  J Physiol. 2007;  580 629-637
  • 13 Barbosa FB, Medina AR, Balbo SL, De Freitas Mathias PC. Low protein diets administered to lactating rats affect in a time-dependent manner the development of young.  Res Commun Mol Pathol Pharmacol. 1999;  106 63-76
  • 14 Lisboa PC, Passos MC, Dutra SC, Bonomo IT, Denolato AT, Reis AM, Moura EG. Leptin and Prolactin, but not Corticosterone, Modulate Body Weight and Thyroid Function in Protein- malnourished Lactating Rats.  Horm Metab Res. 2006;  38 295-299
  • 15 Casanueva FF, Dieguez C. Interaction between body composition, leptin and growth hormone status.  Baillieres Clin Endocrinol Metab. 1998;  12 297-314
  • 16 Aiston S, Agius L. Leptin enhances glycogen storage in hepatocytes by inhibition of phosphorylase and exerts an additive effect with insulin.  Diabetes. 1999;  48 15-20
  • 17 O’Doherty RM, Anderson PR, Zhao AZ, Bornfeldt KE, Newgard CB. Sparing effect of leptin on liver glycogen stores in rats during the fed-to-fasted transition.  Am J Physiol. 1999;  277 ((3 pt 1)) E544-E550
  • 18 Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man.  Diabetologia. 1985;  28 412-419
  • 19 Combs TP, Berg AH, Rajala MW, Klebanov S, Iyengar P, Jimenez-Chillaron JC, Patti ME, Klein SL, Weinstein RS, Scherer PE. Sexual differentiation, pregnancy, calorie restriction, and aging affect adipocyte-specific secretory protein adiponectin.  Diabetes. 2003;  52 268-276
  • 20 Kieffer TJ, Habener JF. The adipoinsular axis:effects of leptin on pancreatic beta-cells.  Am J Physiol Endocrinol Metab. 2000;  278 E1-E14
  • 21 Inoue M, Sakamoto Y, Fujishiro N, Imanaga I, Osaki S, Prestwich GD, Warashina A. Homogeneous Ca+2 stores in rat adrenal chromaffin cells.  Cell Calcium. 2003;  33 19-26
  • 22 Ahren B, Lundquist I, Jarhultm J. Effects of α-1, α-2 and β-adrenoceptor blockers on insulin secretion in the rat.  Acta Endocrinol (Copenh). 1984;  105 78-82
  • 23 Moura AS, Caldeira Filho JS, De Freitas Mathias PC, Franco de Sá CC. Insulin secretion impairment and insulin sensitivity improvement in adult rats undernourished during early lactation.  Res Commun Mol Pathol Pharmacol. 1997;  96 179-192
  • 24 Zambrano E, Bautista CJ, Déas M, Martínez-Samayoa PM, González-Zamorano M, Ledesma H, Morales J, Larrea F, Nathanielsz PW. A low maternal protein diet during pregnancy and lactation has a sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in rat.  J Physiol. 2006;  571 ((pt 1)) 221-230
  • 25 Sampaio de Freitas M, Garcia de Souza EP, Vargas da Silva S, da Rocha Kaezer A, da Silva Vieira R, Sanchez Moura A, Barja-Fidalgo C. Up-regulation of phosphatidylinositol 3-kinase and glucose transporter 4 in muscle of rats subjected to maternal undernutrition.  Biochim Biophys Acta. 2003;  1639 8-16
  • 26 Swarbrick MM, Havel PJ. Physiological, pharmacological, and nutritional regulation of circulating adiponectin concentrations in humans.  Metab Syndr Relat Disord. 2008;  6 87-102
  • 27 Coderre I, Srivastava AK, Chiasson JL. Role of glucocorticoid in the regulation of glycogen metabolism in skeletal muscle.  Am J Physiol Endocr Metab. 1991;  260 927-932
  • 28 Fernandez-Twinn DS, Ozanne SE, Ekizoglou S, Doherty C, James L, Gusterson B, Hales CN. The maternal endocrine environment in the low-protein model of intra-uterine growth restriction.  Br J Nutr. 2003;  90 815-822
  • 29 Boualga A, Bouchenak M, Belleville J. Low-protein diet prevents tissue lipoprotein lipase activity increase in growing rats.  Br J Nutr. 2000;  84 663-667
  • 30 Havel PJ. Control of energy homeostasis and insulin action by adipocyte hormones: leptin, acylation stimulating protein, and adiponectin.  Curr Opin Lipidol. 2002;  13 51-59

Correspondence

Dr. P. C. Lisboa

Departamento de Ciências Fisiológicas – 5° andar

Instituto de Biologia

Universidade do Estado do Rio de Janeiro

Av. 28 de setembro

87- Rio de Janeiro

RJ 20551-030

Brazil

Phone: +21/2587/61 34

Fax: 21/2587/61 29

Email: pclisboa@uerj.br

Email: patricialisboa@pq.cnpq.br