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Protein deficiency during pregnancy and lactation impairs glucose-induced insulin secretion but increases the sensitivity to insulin in weaned rats

Published online by Cambridge University Press:  09 March 2007

Márcia Q. Latorraca ,
Everardo M. Carneiro ,
Antonio C. Boschero  and
Maria A. R. Mello
Márcia Q. Latorraca
Affiliation:
Departamento de Fisiologia e Biofísica, Instituto de Biologia, Universidade Estadual de Campinas, UNICAMP, Campinas, SP, Brazil
Everardo M. Carneiro
Affiliation:
Departamento de Educação Física, Instituto de Biociências, Universidade Estadual Paulista, Rio Claro, SP, Brazil
Antonio C. Boschero*
Affiliation:
Departamento de Fisiologia e Biofísica, Instituto de Biologia, Universidade Estadual de Campinas, UNICAMP, Campinas, SP, Brazil
Maria A. R. Mello
Affiliation:
Departamento de Educação Física, Instituto de Biociências, Universidade Estadual Paulista, Rio Claro, SP, Brazil
*
*Corresponding author: Dr Antonio Carlos Boschero, fax +55 19 289 3124, email [email protected]
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Abstract

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We studied glucose homeostasis in rat pups from dams fed on a normal-protein (170 g/kg) (NP) diet or a diet containing 60 g protein/kg (LP) during fetal life and the suckling period. At birth, total serum protein, serum albumin and serum insulin levels were similar in both groups. However, body weight and serum glucose levels in LP rats were lower than those in NP rats. At the end of the suckling period (28 d of age), total serum protein, serum albumin and serum insulin were significantly lower and the liver glycogen and serum free fatty acid levels were significantly higher in LP rats compared with NP rats. Although the fasting serum glucose level was similar in both groups, the area under the blood glucose concentration curve after a glucose load was higher for NP rats (859 (sem 58) mmol/l per 120 min for NP rats v. 607 (sem 52) mmol/l per 120 min for LP rats; P < 0.005). The mean post-glucose increase in insulin was higher for NP rats (30 (sem 4.7) nmol/l per 120 min for NP rats v. 17 (sem 3.9) nmol/l per 120 min for LP rats; P < 0.05). The glucose disappearance rate for NP rats (0.7 (sem 0.1) %/min) was lower than that for LP rats (1.6 (sem 0.2)%/min; P < 0.001). Insulin secretion from isolated islets (1 h incubation) in response to 16.7mmol glucose/l was augmented 14-fold in NP rats but only 2.6-fold in LP rats compared with the respective basal secretion (2.8 mmol/l; P < 0.001). These results indicate that in vivo as well as in vitro insulin secretion in pups from dams maintained on a LP diet is reduced. This defect may be counteracted by an increase in the sensitivity of target tissues to insulin.

Keywords

Protein malnutritionInsulinGlucose homeostasis
Type
Research Article
Information
British Journal of Nutrition , Volume 80 , Issue 3 , September 1998 , pp. 291 - 297
Copyright
Copyright © The Nutrition Society 1998

References

Alvarez, E & Blásquez, E (1984) Absence of insulin receptor down-regulation in rat hepatocytes during fetal life in rats. Diabetologia 27, 251A.Google Scholar
Blásquez, E, Montoya, E & López Quijada, C (1970) Relationship between insulin concentration in plasma and pancreas of fetal and weanling rats. Journal of Endocrinology 48, 453–461.Google Scholar
Carneiro, EM, Mello, MAR, Gobatto, CA & Boschero, AC (1995) Low protein diet impairs glucose-induced insulin secretion from and 45Ca uptake by pancreatic rat islets. Journal of Nutritional Biochemistry 6, 314–318.CrossRefGoogle Scholar
Crace, CJ, Swenne, I, Kohn, PG, Strain, AJ & Milner, RDG (1990) Protein-energy malnutrition induces changes in insulin sensitivity. Diabete & Metabolisme 16, 484–491.Google Scholar
Dahri, S, Reusens, B, Remacle, C & Hoet, JJ (1995) Nutritional influences on pancreatic development and potential links with non-insulin dependent diabetes. Proceedings of the Nutrition Society 54, 345–356.CrossRefGoogle ScholarPubMed
Dahri, S, Snoeck, A, Reusens-Billen, B, Remacle, C & Hoet, JJ (1991) Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 40, Suppl. 2, 115–120.CrossRefGoogle Scholar
Desai, M, Crowther, NJ, Lucas, A & Hales, CN (1996) Organ-selective growth in the offspring of protein-restricted mothers. British Journal of Nutrition 76, 591–603.CrossRefGoogle ScholarPubMed
Desai, M, Crowther, NJ, Ozanne, SE, Lucas, A & Hales, CN (1995) Adult glucose and lipid metabolism may be programmed during fetal life. Biochemical Society Transactions 23, 331–335.CrossRefGoogle ScholarPubMed
Dixit, PK & Kaung, HLC (1985) Rat pancreatic B-cells in protein deficiency: a study involving morphometric analysis and alloxan effect. Journal of Nutrition 115, 375–381.CrossRefGoogle Scholar
Doumas, BT, Watson, WA & Biggs, HG (1971) Albumin standards and measurements of serum albumin with bromocresol green. Clinica Chimica Acta 31, 87–96.CrossRefGoogle Scholar
Escriva, F, Kergoat, M, Bailbé, D, Pascual-Leone, AM & Portha, B (1991) Increased insulin action in the rat after protein malnutrition early in life. Diabetologia 34, 559–564.CrossRefGoogle ScholarPubMed
Gruppuso, PA, Migliori, R, Susa, JB & Schwartz, R (1981) Chronic maternal hyperinsulinemia and hypoglycemia. A model for experimental intrauterine growth retardation. Biology of the Neonate 40, 113–120.CrossRefGoogle Scholar
Hales, CM & Barker, DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595–601.CrossRefGoogle ScholarPubMed
Hassid, WZ & Abrahams, S (1957) Chemical procedures for analysis of polysaccharides. Methods in Enzymology 3, 34–36.CrossRefGoogle Scholar
Heard, CRC, Frangi, SM, Wright, PM & McCartney, PR (1977) Biochemical characteristics of different forms of protein energy malnutrition: an experimental model using rats. British Journal of Nutrition 37, 1–21.CrossRefGoogle ScholarPubMed
Hill, DJ & Milner, RDG (1980) Increased somatomedins and cartilage metabolic activity in rabbit fetuses injected with insulin in utero. Diabetologia 19, 143–147.CrossRefGoogle ScholarPubMed
Issad, T, Coupe, C, Ferre, P & Girard, J (1987) Insulin resistance during suckling period in rats. American Journal of Physiology 253, E142–E148.Google ScholarPubMed
Langley-Evans, S & Jackson, A (1996) Intrauterine programming of hypertension nutrient–hormone interactions. Nutrition Reviews 54, 163–169.CrossRefGoogle ScholarPubMed
Leeun, R & Vries, IJ (1976) Hypoglycemia in small-for-dates newborn infants. Pediatrics 58, 18–22.Google Scholar
Malaisse, WJ, Malaisse-Lagae, F & Wright, PH (1967) Effect of fasting upon insulin secretion in the rat. American Journal of Physiology 213, 843–848.CrossRefGoogle ScholarPubMed
Matthews, JNS, Altman, DG, Campbell, MJ & Royston, P (1990) Analysis of serial measurements in medical research. British Medical Journal 27, 230–235.CrossRefGoogle Scholar
Mello, MAR, Cury, L, Valle, LBS & Oliveira-Filho, RM (1987) Pregnancy in young rats: effects of malnutrition. Nutrition Reports International 36, 527–535.Google Scholar
Milner, RDG (1971) Metabolic and hormonal responses to glucose and glucagon in patients with infantile malnutrition. Pediatric Research 5, 33–39.CrossRefGoogle Scholar
Okitolonda, W, Brichard, SM & Henquin, JC (1987) Repercussions of chronic protein-calorie malnutrition on glucose homeostasis in the rat. Diabetologia 30, 946–951.CrossRefGoogle ScholarPubMed
Ozanne, SE, Smith, GD, Tikerpae, J & Hales, CN (1996 a) Altered regulation of hepatic glucose output in the male offspring of protein-malnourished dams. American Journal of Physiology 270, E559–E564.Google ScholarPubMed
Ozanne, SE, Wang, CL, Coleman, N & Smith, GD (1996 b) Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. American Journal of Physiology 271, E1128–E1134.Google ScholarPubMed
Rasschaert, J, Reusens, B, Dahri, S, Sener, A, Remacle, C, Hoet, JJ & Malaisse, WJ (1995) Impaired activity of rat pancreatic islets mitochondrial glycerophosphate dehydrogenase in protein malnutrition. Endocrinology 136, 2631–2634.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH & Fahey, GC Jr (1993) AIN-93 purified diets for laboratory rodents: report of the American Institute of Nutrition ad hoc working committee on the reformulation of the AIN-76A rodent diet. Journal of Nutrition 123, 1939–1951.CrossRefGoogle Scholar
Regouw, BJM, Cornelissen, PJHC, Helder, AP, Spijkers, JBV & Weeber, YM (1971) Specific determination of free fatty acid in plasma. Clinica Chimica Acta 31, 187–195.CrossRefGoogle ScholarPubMed
Reis, MAB, Carneiro, EM, Mello, MAR, Boschero, AC, Saad, MJA & Velloso, LA (1997) Glucose-induced insulin secretion is impaired and insulin-induced phosphorylation of the insulin receptor and insulin receptor substrate-1 are increased in proten-deficient rats. Journal of Nutrition 127, 403–410.CrossRefGoogle ScholarPubMed
Reusens, B, Iglesias-Barreira, V, Bennis-Taleb, N, Remacle, C & Hoet, JJ (1997) Effect of an isocaloric low protein diet during gestation on the organ vascularization of the offspring. 16th International Congress of Nutrition, Montreal, Canada, p. 69, Abstr.Google Scholar
Roth, J (1979) Receptors for peptide hormones. In Endocrinology, pp. 2037–2054 [DeGroot, L, editor]. New York: Grune and Stratton.Google Scholar
Sako, Y & Grill, V (1990) A 48-hour lipid infusion in the rat time-dependently inhibits glucose-induced insulin secretion and B-cell oxidation through a process likely coupled to fatty acid oxidation. Endocrinology 127, 1580–1589.CrossRefGoogle ScholarPubMed
Scott, AM, Atwater, I & Rojas, E (1981) A method for the simultaneous measurement of insulin released and B-cell membrane potential in single mouse islets of Langerhans. Diabetologia 21, 470–475.CrossRefGoogle ScholarPubMed
Snoeck, A, Remacle, C, Reusens, B & Hoet, JJ (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biology of the Neonate 57, 107–118.CrossRefGoogle ScholarPubMed
Sokal, RR & Rohlf, FJ (1981) The Principles and Practice of Statistics in Biological Research, pp. 400–453. New York: W.H. Freeman and Co.Google Scholar
Swenne, I, Crace, CJ & Milner, DG (1987) Persistent impairment of insulin secretory response to glucose in adult rats after a limited period of protein-calorie malnutrition early in life. Diabetes 36, 454–458.CrossRefGoogle ScholarPubMed
Trinder, P (1969) Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen. Journal of Clinical Pathology 22, 158–161.CrossRefGoogle ScholarPubMed
Van Assche, FA & Aerts, L (1979) The fetal endocrine pancreas. Contributions to Gynecology and Obstetrics 5, 44–57.CrossRefGoogle ScholarPubMed
Wolfson, WQ, Cohn, C, Calvary, F & Ichiba, F (1948) Studies in serum proteins. 5. A rapid procedure for the estimation of total protein, true albumin, total globulin, alpha globulin, and gamma globulin in 1.0 ml of serum. American Journal of Clinical Pathology 18, 723–730.CrossRefGoogle Scholar
Zhou, YP & Grill, V (1994) Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. Journal of Clinical Investigation 93, 870–876.CrossRefGoogle ScholarPubMed