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The impact of dietary protein restriction on insulin secretion and action

Published online by Cambridge University Press:  28 February 2007

Mark J. Holness
Mark J. Holness*
Affiliation:
Molecular and Cellular Biology, Division of Biomedical Sciences, St Bartholomew’s and the Royal London School of Medicine and Dentistry, Queen Mary and Westfield College, Mile End Road, London E1 4NS, UK
*
Corresponding Author: Dr Mark J. Holness, fax +44 (0)181 981 8836, email m.j.holness@qmw.ac.uk
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Abstract

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The goal of this review is to develop the hypothesis, and review the evidence, that protein restriction, through synergistic effects on multiple organ systems predisposes to loss of normal regulation of fuel homeostasis that plays the central role in the development of type 2 (non-insulin-dependent) diabetes mellitus. The ability of insulin to regulate glucose production and disposal varies between individuals. These differences, together with the various compensatory mechanisms that are invoked to attempt to normalize fuel homeostasis, are of fundamental importance in the development and clinical course of type 2 diabetes mellitus. Protein deprivation impacts on both insulin secretion and insulin action. These effects may persist even when a diet containing adequate protein is presented subsequently. Data are presented that suggest that protein restriction results in an impaired ability of pancreatic β-cells to compensate adequately for the defect in insulin action in insulin-resistant individuals. This persistent impairment of insulin secretion resulting from protein restriction predisposes to loss of glucoregulatory control and impaired insulin action after the subsequent imposition of a diabetogenic challenge. This inability to maintain the degree of compensatory hyperinsulinaemia necessary to prevent loss of glucose tolerance may have relevance to the increased incidence of diabetes on changing from a nutritionally-poor diet to a Western diet, and to the hypothesis that some cases of type 2 diabetes in adulthood may be related to poor early nutrition.

Keywords

Protein restrictionFetal programmingNon-insulin-dependent diabetes mellitusInsulin resistance
Type
Sir David Cuthbertson Medal Lecture
Information
Proceedings of the Nutrition Society , Volume 58 , Issue 3 , August 1999 , pp. 647 - 653
Copyright
Copyright © The Nutrition Society 1999

References

Barker, DJP, Hales, CN, Fall, CH, Osmond, C, Phipps, K & Clark, PM (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62–67.Google Scholar
Becker, DJ (1983) The endocrine responses to protein calorie malnutrition. Annual Review of Nutrition 3, 187–212.CrossRefGoogle ScholarPubMed
Becker, DJ, Pimstone, BL, Hansen, JD & Hendricks, S (1971) Insulin secretion in protein-calorie malnutrition. I. Quantitative abnormalities and response to treatment. Diabetes 20, 542–551.CrossRefGoogle ScholarPubMed
Bowie, MD (1964) Intravenous glucose tolerance in kwashiorkor and marasmus. South African Medical Journal 38, 328–329.Google Scholar
Cherif, H, Reusens, B, Ahn, MT, Hoet, JJ & Remacle, C (1998) Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. Journal of Endocrinology 159, 341–348.Google Scholar
Cohen, MP, Stern, E, Rusecki, Y & Zeidler, A (1988) High prevalence of diabetes in young adult Ethiopian immigrants to Israel. Diabetes 37, 824–828.Google Scholar
Collins, VR, Dowse, GK, Toelupe, PM, Imo, TT, Aloaina, FL, Spark, RA & Zimmet, PZ (1994) Increasing prevalence of NIDDM in the Pacific island population of Western Samoa over a 13-year period. Diabetes Care 17, 288–296.Google Scholar
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.Google Scholar
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.Google Scholar
Dollet, JM, Beck, B, Villaume, C, Max, JP & Debry, G (1985) Progressive adaptation of the endocrine pancreas during long-term protein deficiency in rats: effects on blood glucose homeostasis and on pancreatic insulin, glucagon and somatostatin concentrations. Journal of Nutrition 115, 1581–1588.Google Scholar
Dowse, GK, Zimmet, PZ, Finch, CF & Collins, VR (1991) Decline in incidence of epidemic glucose intolerance in Nauruans: implications for the ‘thrifty genotype’. American Journal of Epidemiology 133, 1093–1104.CrossRefGoogle ScholarPubMed
Escriva, F, Kergoat, M, Bailbe, D, Pascual-Leone, AM & Portha, B (1991) Increased insulin action in the rat after protein malnutrition early in life. Diabetologia 34, 559–564.Google Scholar
Habicht, JP, Lechtig, A, Yarbrough, C & Klein, RE (1974) Maternal nutrition, birth weight and infant mortality. In Size at Birth. Ciba Foundation Symposium no. 27, pp. 353–377. Amsterdam: Excerpta Medica.Google Scholar
Hales, CN (1997) Fetal and infant growth and impaired glucose tolerance in adulthood: the ‘thrifty phenotype’ hypothesis revisited. Acta Paediatrica 422, Suppl., 73–77.Google Scholar
Hales, CN & Barker, DJP (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595–601.Google Scholar
Hales, CN, Barker, DJP, Clark, PM, Cox, LJ, Fall, C, Osmond, C & Winter, PD (1991) Fetal and infant growth and impaired glucose tolerance at age 64. British Medical Journal 303, 1019–1022.CrossRefGoogle ScholarPubMed
Hales, CN, Desai, M, Ozanne, S & Crowther, NJ (1996) Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochemical Society Transactions 24, 341–350.CrossRefGoogle Scholar
Holness, MJ (1996 a) The influence of sub-optimal protein nutrition on insulin hypersecretion evoked by high-energy/high-fat feeding in rats. FEBS Letters 396, 53–56.CrossRefGoogle ScholarPubMed
Holness, MJ (1996 b) Impact of early growth retardation on glucoregulatory control and insulin action in mature rats. American Journal of Physiology 270, E946–E954.Google ScholarPubMed
Holness, MJ, Fryer, LGD, Priestman, DA & Sugden, MC (1998) Moderate protein restriction during pregnancy modifies the regulation of triacylglycerol turnover by insulin and leads to dysregulation of insulin’s anti-lipolytic action. Molecular and Cellular Endocrinology 142, 25–33.Google Scholar
Holness, MJ & Sugden, MC (1990) Glucose utilization in heart, diaphragm and skeletal muscle during the fed-to-starved transition. Biochemical Journal 270, 245–249.Google Scholar
Holness, MJ & Sugden, MC (1996) Suboptimal protein nutrition in early life later influences insulin action in pregnant rats. Diabetologia 39, 12–21.Google Scholar
Holness, MJ & Sugden, MC (1999) Antecedent protein restriction exacerbates the development of impaired insulin action after high-fat feeding. American Journal of Physiology 276, E85–E93.Google ScholarPubMed
Levine, LS, Wright, PG & Marcus, F (1983) Failure to secrete immunoreactive insulin by rats fed a low protein diet. Acta Endocrinologica 102, 240–245.Google ScholarPubMed
Lumey, LH (1992) Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 1944–1945. Paediatric and Perinatal Epidemiology 6, 240–253.Google Scholar
Milner, RDG (1971) Metabolic and hormonal responses to glucose and glucagon in patients with infantile malnutrition. Pediatric Research 5, 33–39.Google Scholar
Nolan, CJ & Proietto, J (1994) The feto-placental glucose steal phenomenon is a major cause of maternal metabolic adaptation during late pregnancy in the rat. Diabetologia 37, 976–984.Google Scholar
Nolan, CJ & Proietto, J (1996) The set point for maternal glucose homeostasis is lowered during late pregnancy in the rat: the role of the islet beta-cell and liver. Diabetologia 39, 785–792.Google Scholar
Okitolonda, W, Brichard, SM & Henquin, JC (1987) Repercussions of chronic protein-calorie malnutrition on glucose homeostasis in the rat. Diabetologia 30, 946–951.Google Scholar
Ozanne, SE, Nave, BT, Wang, CL, Shepherd, PR, Prins, J & Smith, GD (1997) Poor fetal nutrition causes long-term changes in expression of insulin signaling components in adipocytes. American Journal of Physiology 273, E46–E51.Google Scholar
Ozanne, SE, Wang, CL, Coleman, N & Smith, GD (1996) Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. American Journal of Physiology 271, E1128–E1134.Google Scholar
Petry, CJ, Desai, M, Ozanne, SE & Hales, CN (1997) Early and late nutritional windows for diabetes susceptibility. Proceedings of the Nutrition Society 56, 233–242.Google Scholar
Phillips, DIW (1996) Insulin resistance as a programmed response to fetal undernutrition. Diabetologia 39, 1119–1122.Google Scholar
Picarel-Blanchot, F, Alvarez, C, Bailbe, D, Pascual-Leone, AM & Portha, B (1995) 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 44, 1519–1526.CrossRefGoogle ScholarPubMed
Rao, RH (1988) Diabetes in the undernourished: coincidence or consequence? Endocrine Reviews 9, 67–87.Google Scholar
Rasschaert, J, Reusens, B, Dahri, S, Sener, A, Remacle, C, Hoet, JJ & Malaisse, WJ (1995) Impaired activity of rat pancreatic islet mitochondrial glycerophosphate dehydrogenase in protein malnutrition. Endocrinology 136, 2631–2634.Google Scholar
Reaven, GM (1995 a) The fourth musketeer - from Alexandre Dumas to Claude Bernard. Diabetologia 38, 3–13.Google Scholar
Reaven, GM (1995 b) Pathophysiology of insulin resistance in human disease. Physiological Reviews 75, 473–486.Google Scholar
Sener, A, Reusens, B, Remacle, C, Hoet, JJ & Malaisse, WJ (1996) Nutrient metabolism in pancreatic islets from protein malnourished rats. Biochemical and Molecular Medicine 59, 62–67.Google Scholar
Shepherd, PR, Crowther, NJ, Desai, M, Hales, CN & Ozanne, SE (1997) Altered adipocyte properties in the offspring of protein malnourished rats. British Journal of Nutrition 78, 121–129.Google Scholar
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
Sorenson, RL & Brelje, TC (1997) Adaptation of islets of Langerhans to pregnancy: beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones. Hormone and Metabolic Research 29, 301–307.Google Scholar
Sugden, MC, Fryer, LG & Holness, MJ (1996) Regulation of hepatic pyruvate dehydrogenase kinase by insulin and dietary manipulation in vivo. Studies with the euglycaemic-hyperinsulinaemic clamp. Biochimica et Biophysica Acta 1316, 114–120.Google Scholar
Sugden, MC & Holness, MJ (1995) Modulation of in vivo insulin action by dietary protein during pregnancy. American Journal of Physiology 268, E722–E729.Google ScholarPubMed
Swenne, I, Borg, LA, Crace, CJ & Schnell, Landstrom A (1992) Persistent reduction of pancreatic beta-cell mass after a limited period of protein-energy malnutrition in the young rat. Diabetologia 35, 939–945.CrossRefGoogle ScholarPubMed
Swenne, I, Crace, CJ & Milner, RD (1987) Persistent impairment of insulin secretory response to glucose in adult rats after limited period of protein-calorie malnutrition early in life. Diabetes 36, 454–458.Google Scholar
Van Assche, FA (1975) Foetal endocrine pancreas. In Carbohydrate Metabolism in Pregnancy and the Newborn, pp. 68–82 [Sutherland, HW and Stowers, JM, editors]. Edinburgh: Churchill Livingstone.Google Scholar
World Health Organization (1985) Diabetes Mellitus. Technical Report Series no. 727, pp. 20–25. Geneva: WHO.Google Scholar
Wilson, MR & Hughes, SJ (1997) The effect of maternal protein deficiency during pregnancy and lactation on glucose tolerance and pancreatic islet function in adult rat offspring. Journal of Endocrinology 154, 177–185.Google Scholar