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Nutrition & Metabolism
Published in: Nutrition & Metabolism 1/2012

Open Access 01-12-2012 | Review

Early postnatal low-protein nutrition, metabolic programming and the autonomic nervous system in adult life

Authors: Júlio Cezar de Oliveira, Sabrina Grassiolli, Clarice Gravena, Paulo Cezar Freitas de Mathias

Published in: Nutrition & Metabolism | Issue 1/2012

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Abstract

Protein restriction during lactation has been used as a rat model of metabolic programming to study the impact of perinatal malnutrition on adult metabolism. In contrast to protein restriction during fetal life, protein restriction during lactation did not appear to cause either obesity or the hallmarks of metabolic syndrome, such as hyperinsulinemia, when individuals reached adulthood. However, protein restriction provokes body underweight and hypoinsulinemia. This review is focused on the regulation of insulin secretion and the influence of the autonomic nervous system (ANS) in adult rats that were protein-malnourished during lactation. The data available on the topic suggest that the perinatal phase of lactation, when insulted by protein deficit, imprints the adult metabolism and thereby alters the glycemic control. Although hypoinsulinemia programs adult rats to maintain normoglycemia, pancreatic β-cells are less sensitive to secretion stimuli, such as glucose and cholinergic agents. These pancreatic dysfunctions may be attributed to an imbalance of ANS activity recorded in adult rats that experienced maternal protein restriction.
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Literature
1.
Hales CN, Barker DJ: The thrifty phenotype hypothesis. Br Med Bull. 2001, 60: 5-20. 10.1093/bmb/60.1.5.CrossRef
2.
Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD: Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991, 303: 1019-1022. 10.1136/bmj.303.6809.1019.CrossRef
3.
Molendi-Coste O, Laborie C, Scarpa MC, Montel V, Vieau D, Breton C: Maternal perinatal undernutrition alters postnatal development of chromaffin cells in the male rat adrenal medulla. Neuroendocrinology. 2009, 90: 54-66. 10.1159/000209222.CrossRef
4.
Sullivan EL, Grove KL: Metabolic imprinting in obesity. Forum Nutr. 2010, 63: 186-194.CrossRef
5.
de Oliveira JC, Scomparin DX, Andreazzi AE, Branco RC, Martins AG, Gravena C, Grassiolli S, Rinaldi W, Barbosa FB, Mathias PC: Metabolic imprinting by maternal protein malnourishment impairs vagal activity in adult rats. J Neuroendocrinol. 2011, 23: 148-157. 10.1111/j.1365-2826.2010.02095.x.CrossRef
6.
Kimani-Murage EW, Kahn K, Pettifor JM, Tollman SM, Dunger DB, Gomez-Olive XF, Norris SA: The prevalence of stunting, overweight and obesity, and metabolic disease risk in rural South African children. BMC Publ Health. 2010, 10: 158-10.1186/1471-2458-10-158.CrossRef
7.
Sawaya AL, Roberts S: Stunting and future risk of obesity: principal physiological mechanisms. Cad Saude Publica. 2003, 19 (Suppl 1): S21-S28.CrossRef
8.
Moura AS, Carpinelli AR, Barbosa FB, Gravena C, Mathias PC: Undernutrition during early lactation as an alternative model to study the onset of diabetes mellitus type II. Res Commun Mol Pathol Pharmacol. 1996, 92: 73-84.
9.
Lesage J, Sebaai N, Leonhardt M, Dutriez-Casteloot I, Breton C, Deloof S, Vieau D: Perinatal maternal undernutrition programs the offspring hypothalamo-pituitary-adrenal (HPA) axis. Stress. 2006, 9: 183-198. 10.1080/10253890601056192.CrossRef
10.
Shimazu T: Central nervous system regulation of liver and adipose tissue metabolism. Diabetologia. 1981, 20 (Suppl): 343-356.CrossRef
11.
Ishikawa K, Shimazu T: Circadian rhythm of liver glycogen metabolism in rats: effects of hypothalamic lesions. Am J Physiol. 1980, 238: E21-E25.
12.
Shimazu T: Innervation of the liver and glucoregulation: roles of the hypothalamus and autonomic nerves. Nutrition. 1996, 12: 65-66.
13.
Nagai K, Nagai N, Shimizu K, Chun S, Nakagawa H, Niijima A: SCN output drives the autonomic nervous system: with special reference to the autonomic function related to the regulation of glucose metabolism. Prog Brain Res. 1996, 111: 253-272.CrossRef
14.
Ahren B: Regulation of insulin secretion by nerves and neuropeptides. Ann Acad Med Singapore. 1999, 28: 99-104.
15.
Wilke RA, Hillard CJ: Decreased adrenal medullary catecholamine release in spontaneously diabetic BB-Wistar rats. Role of hypoglycemia. Diabetes. 1994, 43: 724-729. 10.2337/diabetes.43.5.724.CrossRef
16.
Gilon P, Henquin JC: Mechanisms and physiological significance of the cholinergic control of pancreatic beta-cell function. Endocr Rev. 2001, 22: 565-604. 10.1210/er.22.5.565.
17.
Chesnut RM, Gautille T, Blunt BA, Klauber MR, Marshall LF: Neurogenic hypotension in patients with severe head injuries. J Trauma. 1998, 44: 958-963. 10.1097/00005373-199806000-00003. discussion 963-954CrossRef
18.
Tew EM, Fearon A, Anderson PN, Burnstock G: Tyrosine hydroxylase-containing fibres extend from the rat corpus striatum into grafts of muscularis externa and myenteric plexus. Neurosci Lett. 1995, 194: 33-36. 10.1016/0304-3940(95)11714-8.CrossRef
19.
Ahren B: Autonomic regulation of islet hormone secretion–implications for health and disease. Diabetologia. 2000, 43: 393-410. 10.1007/s001250051322.CrossRef
20.
Inoue S, Bray GA: An autonomic hypothesis for hypothalamic obesity. Life Sci. 1979, 25: 561-566. 10.1016/0024-3205(79)90549-6.CrossRef
21.
Rohner-Jeanrenaud F: Neuroendocrine regulation of nutrient partitioning. Ann N Y Acad Sci. 1999, 892: 261-271. 10.1111/j.1749-6632.1999.tb07800.x.CrossRef
22.
Scomparin DX, Gomes RM, Grassiolli S, Rinaldi W, Martins AG, de Oliveira JC, Gravena C, de Freitas Mathias PC: Autonomic activity and glycemic homeostasis are maintained by precocious and low intensity training exercises in MSG-programmed obese mice. Endocrine. 2009, 36: 510-517. 10.1007/s12020-009-9263-2.CrossRef
23.
Vozarova De Courten B, Weyer C, Stefan N, Horton M, DelParigi A, Havel P, Bogardus C, Tataranni PA: Parasympathetic blockade attenuates augmented pancreatic polypeptide but not insulin secretion in Pima Indians. Diabetes. 2004, 53: 663-671. 10.2337/diabetes.53.3.663.CrossRef
24.
Ferreira F, Filiputti E, Arantes VC, Stoppiglia LF, Araujo EP, Delghingaro-Augusto V, Latorraca MQ, Toyama MH, Boschero AC, Carneiro EM: Decreased cholinergic stimulation of insulin secretion by islets from rats fed a low protein diet is associated with reduced protein kinase calpha expression. J Nutr. 2003, 133: 695-699.
25.
Leon-Quinto T, Magnan C, Portha B: Altered activity of the autonomous nervous system as a determinant of the impaired beta-cell secretory response after protein-energy restriction in the rat. Endocrinology. 1998, 139: 3382-3389. 10.1210/en.139.8.3382.
26.
Tataranni PA: From physiology to neuroendocrinology: a reappraisal of risk factors of body weight gain in humans. Diabetes Metab. 1998, 24: 108-115.
27.
James WP: The epidemiology of obesity: the size of the problem. J Intern Med. 2008, 263: 336-352. 10.1111/j.1365-2796.2008.01922.x.CrossRef
28.
Hallal PC, Azevedo MR, Reichert FF, Siqueira FV, Araujo CL, Victora CG: Who, when, and how much? Epidemiology of walking in a middle-income country. Am J Prev Med. 2005, 28: 156-161. 10.1016/j.amepre.2004.10.012.CrossRef
29.
Bunag RD, Takeda K: Sympathetic hyperresponsiveness to hypothalamic stimulation in young hypertensive rats. Am J Physiol. 1979, 237: R39-R44.
30.
Cano G, Card JP, Sved AF: Dual viral transneuronal tracing of central autonomic circuits involved in the innervation of the two kidneys in rat. J Comp Neurol. 2004, 471: 462-481. 10.1002/cne.20040.CrossRef
31.
Lucas A: Programming by early nutrition: an experimental approach. J Nutr. 1998, 128: 401S-406S.
32.
Heindel JJ, Vom Saal FS: Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity. Mol Cell Endocrinol. 2009, 304: 90-96. 10.1016/j.mce.2009.02.025.CrossRef
33.
Bird A: DNA methylation patterns and epigenetic memory. Genes Dev. 2002, 16: 6-21. 10.1101/gad.947102.CrossRef
34.
Burdge GC, Hanson MA, Slater-Jefferies JL, Lillycrop KA: Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life?. Br J Nutr. 2007, 97: 1036-1046. 10.1017/S0007114507682920.CrossRef
35.
Guilloteau P, Zabielski R, Hammon HM, Metges CC: Adverse effects of nutritional programming during prenatal and early postnatal life, some aspects of regulation and potential prevention and treatments. J Physiol Pharmacol. 2009, 60 (Suppl 3): 17-35.
36.
Attig L, Gabory A, Junien C: Early nutrition and epigenetic programming: chasing shadows. Curr Opin Clin Nutr Metab Care. 2010, 13: 284-293. 10.1097/MCO.0b013e328338aa61.CrossRef
37.
Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH: Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008, 105: 17046-17049. 10.1073/pnas.0806560105.CrossRef
38.
Park JH, Stoffers DA, Nicholls RD, Simmons RA: Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest. 2008, 118: 2316-2324.CrossRef
39.
Holness MJ, Langdown ML, Sugden MC: Early-life programming of susceptibility to dysregulation of glucose metabolism and the development of Type 2 diabetes mellitus. Biochem J. 2000, 349 (Pt 3): 657-665.CrossRef
40.
Chang-Chen KJ, Mullur R, Bernal-Mizrachi E: Beta-cell failure as a complication of diabetes. Rev Endocr Metab Disord. 2008, 9: 329-343. 10.1007/s11154-008-9101-5.CrossRef
41.
Barker DJ: The developmental origins of chronic adult disease. Acta Paediatr Suppl. 2004, 93: 26-33.CrossRef
42.
Sawaya AL, Martins PA, Grillo LP, Florencio TT: Long-term effects of early malnutrition on body weight regulation. Nutr Rev. 2004, 62: S127-S133.CrossRef
43.
Plagemann A, Harder T, Dudenhausen JW: The diabetic pregnancy, macrosomia, and perinatal nutritional programming. Nestle Nutr Workshop Ser Pediatr Program. 2008, 61: 91-102.CrossRef
44.
Wainford RD, Kapusta DR: Chronic high-NaCl intake prolongs the cardiorenal responses to central N/OFQ and produces regional changes in the endogenous brain NOP receptor system. Am J Physiol Regul Integr Comp Physiol. 2009, 296: R280-R288.CrossRef
45.
Ito K, Kimura Y, Hirooka Y, Sagara Y, Sunagawa K: Activation of Rho-kinase in the brainstem enhances sympathetic drive in mice with heart failure. Auton Neurosci. 2008, 142: 77-81. 10.1016/j.autneu.2008.07.010.CrossRef
46.
Ciriello J, Solano-Flores LP, Rosas-Arellano MP, Kirouac GJ, Babic T: Medullary pathways mediating the parasubthalamic nucleus depressor response. Am J Physiol Regul Integr Comp Physiol. 2008, 294: R1276-R1284. 10.1152/ajpregu.00437.2007.CrossRef
47.
Khadilkar VV, Cameron FJ, Stanhope R: Growth failure and pituitary function in CHARGE and VATER associations. Arch Dis Child. 1999, 80: 167-170. 10.1136/adc.80.2.167.CrossRef
48.
Mitrani P, Srinivasan M, Dodds C, Patel MS: Role of the autonomic nervous system in the development of hyperinsulinemia by high-carbohydrate formula feeding to neonatal rats. Am J Physiol Endocrinol Metab. 2007, 292: E1069-E1078.CrossRef
49.
Young JB: Developmental origins of obesity: a sympathoadrenal perspective. Int J Obes (Lond). 2006, 30 (Suppl 4): S41-S49.CrossRef
50.
Moura AS, Caldeira Filho JS, de Freitas Mathias PC, de Sa CC: Insulin secretion impairment and insulin sensitivity improvement in adult rats undernourished during early lactation. Res Commun Mol Pathol Pharmacol. 1997, 96: 179-192.
51.
Martins PA, Sawaya AL: Evidence for impaired insulin production and higher sensitivity in stunted children living in slums. Br J Nutr. 2006, 95: 996-1001. 10.1079/BJN20061754.CrossRef
52.
Barbosa FB, Gravena C, Mathias P, Moura AS: Blockade of the 32P phosphate flush of pancreatic beta cells from adult rats who received a low-protein diet during early lactation. Braz J Med Biol Res. 1993, 26: 1355-1358.
53.
Gravena C, Andreazzi AE, Mecabo FT, Grassiolli S, Scantamburlo VM, Mathias PC: Protein restriction during lactation alters the autonomic nervous system control on glucose-induced insulin secretion in adult rats. Nutr Neurosci. 2007, 10: 79-87. 10.1080/10284150701308693.CrossRef
54.
Gravena C, Mathias PC, Ashcroft SJ: Acute effects of fatty acids on insulin secretion from rat and human islets of Langerhans. J Endocrinol. 2002, 173: 73-80. 10.1677/joe.0.1730073.CrossRef
55.
Reusens B, Remacle C: Programming of the endocrine pancreas by the early nutritional environment. Int J Biochem Cell Biol. 2006, 38: 913-922. 10.1016/j.biocel.2005.10.012.CrossRef
56.
Sebaai N, Lesage J, Breton C, Vieau D, Deloof S: Perinatal food deprivation induces marked alterations of the hypothalamo-pituitary-adrenal axis in 8-month-old male rats both under basal conditions and after a dehydration period. Neuroendocrinology. 2004, 79: 163-173. 10.1159/000078098.CrossRef
57.
Laborie C, Molendi-Coste O, Breton C, Montel V, Vandenbulcke F, Grumolato L, Anouar Y, Vieau D: Maternal perinatal undernutrition has long-term consequences on morphology, function and gene expression of the adrenal medulla in the adult male rat. J Neuroendocrinol. 2011, 23: 711-724. 10.1111/j.1365-2826.2011.02159.x.CrossRef
58.
Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD: Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab. 2000, 279: E83-E87.
59.
Breton C, Lukaszewski MA, Risold PY, Enache M, Guillemot J, Riviere G, Delahaye F, Lesage J, Dutriez-Casteloot I, Laborie C, Vieau D: Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. Am J Physiol Endocrinol Metab. 2009, 296: E462-E472.CrossRef
60.
Bassett DR, Craig BW: Influence of early nutrition on growth and adipose tissue characteristics in male and female rats. J Appl Physiol. 1988, 64: 1249-1256. 10.1063/1.342505.CrossRef
61.
Gabory A, Attig L, Junien C: Sexual dimorphism in environmental epigenetic programming. Mol Cell Endocrinol. 2009, 304: 8-18. 10.1016/j.mce.2009.02.015.CrossRef
62.
Loizzo S, Vella S, Loizzo A, Fortuna A, Di Biase A, Salvati S, Frajese GV, Agrapart V, Ramirez Morales R, Spampinato S: Sexual dimorphic evolution of metabolic programming in non-genetic non-alimentary mild metabolic syndrome model in mice depends on feed-back mechanisms integrity for pro-opiomelanocortin-derived endogenous substances. Peptides. 2010, 31: 1598-1605. 10.1016/j.peptides.2010.05.006.CrossRef
63.
Moura AS, Franco De Sa CC, Lopez Da Costa C, Vicente LL, Guerreiro SM, Pinto AM: Association between nutrition and gender during lactation influencing glucose homeostasis and blood pressure of the adult offspring. Biol Neonate. 2002, 82: 263-270. 10.1159/000065889.CrossRef
64.
Sugden MC, Holness MJ: Gender-specific programming of insulin secretion and action. J Endocrinol. 2002, 175: 757-767. 10.1677/joe.0.1750757.CrossRef
65.
Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN, Ozanne SE: 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.CrossRef
66.
Zambrano E, Bautista CJ, Deas M, Martinez-Samayoa PM, Gonzalez-Zamorano M, Ledesma H, Morales J, Larrea F, Nathanielsz PW: 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.CrossRef
67.
Zambrano E, Martinez-Samayoa PM, Bautista CJ, Deas M, Guillen L, Rodriguez-Gonzalez GL, Guzman C, Larrea F, Nathanielsz PW: Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol. 2005, 566: 225-236. 10.1113/jphysiol.2005.086462.CrossRef
68.
Sener A, Malaisse WJ: The stimulus-secretion coupling of amino acid-induced insulin release: insulinotropic action of branched-chain amino acids at physiological concentrations of glucose and glutamine. Eur J Clin Invest. 1981, 11: 455-460. 10.1111/j.1365-2362.1981.tb02013.x.CrossRef
69.
Morgan D, Rebelato E, Abdulkader F, Graciano MF, Oliveira-Emilio HR, Hirata AE, Rocha MS, Bordin S, Curi R, Carpinelli AR: Association of NAD(P)H oxidase with glucose-induced insulin secretion by pancreatic beta-cells. Endocrinology. 2009, 150: 2197-2201.CrossRef
70.
Ashcroft FM, Ashcroft SJ, Harrison DE: Effects of 2-ketoisocaproate on insulin release and single potassium channel activity in dispersed rat pancreatic beta-cells. J Physiol. 1987, 385: 517-529.CrossRef
71.
Chistiakov DA, Potapov VA, Khodirev DC, Shamkhalova MS, Shestakova MV, Nosikov VV: Genetic variations in the pancreatic ATP-sensitive potassium channel, beta-cell dysfunction, and susceptibility to type 2 diabetes. Acta Diabetol. 2009, 46: 43-49. 10.1007/s00592-008-0056-5.CrossRef
72.
Henquin JC: Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes. 2000, 49: 1751-1760. 10.2337/diabetes.49.11.1751.CrossRef
73.
Barbosa FB, Capito K, Kofod H, Thams P: Pancreatic islet insulin secretion and metabolism in adult rats malnourished during neonatal life. Br J Nutr. 2002, 87: 147-155. 10.1079/BJN2001489.CrossRef
74.
Branco RC, de Oliveira JC, Grassiolli S, Miranda RA, Barella LF, Gomes RM, Bataglini LA, Torrezan R, Gravena C, de Freitas Mathias PC: Maternal protein malnutrition does not impair insulin secretion from pancreatic islets of offspring after transplantation into diabetic rats. PLoS One. 2012, 7: e30685-10.1371/journal.pone.0030685.CrossRef
75.
Ahren B, Wierup N, Sundler F: Neuropeptides and the regulation of islet function. Diabetes. 2006, 55 (Suppl 2): S98-S107.CrossRef
76.
Caulfield MP: Muscarinic receptors–characterization, coupling and function. Pharmacol Ther. 1993, 58: 319-379. 10.1016/0163-7258(93)90027-B.CrossRef
77.
Bonner TI, Young AC, Brann MR, Buckley NJ: Cloning and expression of the human and rat m5 muscarinic acetylcholine receptor genes. Neuron. 1988, 1: 403-410. 10.1016/0896-6273(88)90190-0.CrossRef
78.
Miguel JC, Abdel-Wahab YH, Mathias PC, Flatt PR: Muscarinic receptor subtypes mediate stimulatory and paradoxical inhibitory effects on an insulin-secreting beta cell line. Biochim Biophys Acta. 2002, 1569: 45-50. 10.1016/S0304-4165(01)00232-X.CrossRef
79.
Iismaa TP, Kerr EA, Wilson JR, Carpenter L, Sims N, Biden TJ: Quantitative and functional characterization of muscarinic receptor subtypes in insulin-secreting cell lines and rat pancreatic islets. Diabetes. 2000, 49: 392-398. 10.2337/diabetes.49.3.392.CrossRef
80.
Balakrishnan S, Mathew J, Antony S, Paulose CS: Muscarinic M(1), M(3) receptors function in the brainstem of streptozotocin induced diabetic rats: their role in insulin secretion from the pancreatic islets as a function of age. Eur J Pharmacol. 2009, 608: 14-22. 10.1016/j.ejphar.2009.01.047.CrossRef
81.
Boschero AC, Szpak-Glasman M, Carneiro EM, Bordin S, Paul I, Rojas E, Atwater I: Oxotremorine-m potentiation of glucose-induced insulin release from rat islets involves M3 muscarinic receptors. Am J Physiol. 1995, 268: E336-E342.
82.
Yamada M, Miyakawa T, Duttaroy A, Yamanaka A, Moriguchi T, Makita R, Ogawa M, Chou CJ, Xia B, Crawley JN: Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Nature. 2001, 410: 207-212. 10.1038/35065604.CrossRef
83.
Duttaroy A, Zimliki CL, Gautam D, Cui Y, Mears D, Wess J: Muscarinic stimulation of pancreatic insulin and glucagon release is abolished in m3 muscarinic acetylcholine receptor-deficient mice. Diabetes. 2004, 53: 1714-1720. 10.2337/diabetes.53.7.1714.CrossRef
84.
Gautam D, Ruiz De Azua I, Li JH, Guettier JM, Heard T, Cui Y, Lu H, Jou W, Gavrilova O, Zawalich WS, Wess J: Beneficial metabolic effects caused by persistent activation of beta-cell M3 muscarinic acetylcholine receptors in transgenic mice. Endocrinology. 2010, 151: 5185-5194. 10.1210/en.2010-0519.CrossRef
85.
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 body composition and glucose homeostasis in the adult rat offspring. Br J Nutr. 2007, 98: 922-928.CrossRef
86.
Fisher RS, Buchwald NA, Hull CD, Levine MS: GABAergic basal forebrain neurons project to the neocortex: the localization of glutamic acid decarboxylase and choline acetyltransferase in feline corticopetal neurons. J Comp Neurol. 1988, 272: 489-502. 10.1002/cne.902720404.CrossRef
87.
Markakis EA: Development of the neuroendocrine hypothalamus. Front Neuroendocrinol. 2002, 23: 257-291. 10.1016/S0091-3022(02)00003-1.CrossRef
Metadata
Title
Early postnatal low-protein nutrition, metabolic programming and the autonomic nervous system in adult life
Authors
Júlio Cezar de Oliveira
Sabrina Grassiolli
Clarice Gravena
Paulo Cezar Freitas de Mathias
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Nutrition & Metabolism / Issue 1/2012
Electronic ISSN: 1743-7075
DOI
https://doi.org/10.1186/1743-7075-9-80

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