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

Nutrition and Metabolism

Volumn 9, Issue , 2012, Pages

  De Oliveira, Júlio Cezar ^a   Grassiolli, Sabrina ^b   Gravena, Clarice ^a   De Mathias, Paulo Cezar Freitas ^a  

^a STATE UNIVERSITY OF MARINGÁ   (Brazil)

^b STATE UNIVERSITY OF PONTA GROSSA   (Brazil)

Author keywords

Autonomic nervous system; Insulin secretion; Lactation; Metabolic programming; Pancreatic islets

Indexed keywords

CHOLINERGIC RECEPTOR STIMULATING AGENT; GLUCOSE; INSULIN; NEUROTRANSMITTER;

AUTONOMIC NERVOUS SYSTEM FUNCTION; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; HYPOINSULINEMIA; INSULIN RELEASE; LACTATION; METABOLISM; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PROTEIN DEFICIENCY; REVIEW; SEX DIFFERENCE;

RATTUS;

EID: 84865981064     PISSN: None     EISSN: 17437075     Source Type: Journal    
DOI: 10.1186/1743-7075-9-80     Document Type: Review

References (87)

1. The thrifty phenotype hypothesis. Hales CN, Barker DJ, Br Med Bull 2001 60 5 20 10.1093/bmb/60.1.5 11809615
2. Fetal and infant growth and impaired glucose tolerance at age 64. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD, BMJ 1991 303 1019 1022 10.1136/bmj.303.6809.1019 1954451
3. Maternal perinatal undernutrition alters postnatal development of chromaffin cells in the male rat adrenal medulla. Molendi-Coste O, Laborie C, Scarpa MC, Montel V, Vieau D, Breton C, Neuroendocrinology 2009 90 54 66 10.1159/000209222 19276635
4. Metabolic imprinting in obesity. Sullivan EL, Grove KL, Forum Nutr 2010 63 186 194 19955786
5. Metabolic imprinting by maternal protein malnourishment impairs vagal activity in adult rats. de Oliveira JC, Scomparin DX, Andreazzi AE, Branco RC, Martins AG, Gravena C, Grassiolli S, Rinaldi W, Barbosa FB, Mathias PC, J Neuroendocrinol 2011 23 148 157 10.1111/j.1365-2826.2010.02095.x 21091554
6. The prevalence of stunting, overweight and obesity, and metabolic disease risk in rural South African children. Kimani-Murage EW, Kahn K, Pettifor JM, Tollman SM, Dunger DB, Gomez-Olive XF, Norris SA, BMC Publ Health 2010 10 158 10.1186/1471-2458-10-158
7. Stunting and future risk of obesity: principal physiological mechanisms. Sawaya AL, Roberts S, Cad Saude Publica 2003 19 Suppl 1 21 S28 12886432
8. Undernutrition during early lactation as an alternative model to study the onset of diabetes mellitus type II. Moura AS, Carpinelli AR, Barbosa FB, Gravena C, Mathias PC, Res Commun Mol Pathol Pharmacol 1996 92 73 84 8733829
9. Perinatal maternal undernutrition programs the offspring hypothalamo-pituitary-adrenal (HPA) axis. Lesage J, Sebaai N, Leonhardt M, Dutriez-Casteloot I, Breton C, Deloof S, Vieau D, Stress 2006 9 183 198 10.1080/10253890601056192 17175504
10. Central nervous system regulation of liver and adipose tissue metabolism. Shimazu T, Diabetologia 1981 20 Suppl 343 356 7014330
11. Circadian rhythm of liver glycogen metabolism in rats: effects of hypothalamic lesions. Ishikawa K, Shimazu T, Am J Physiol 1980 238 21 E25 6766673
12. Innervation of the liver and glucoregulation: roles of the hypothalamus and autonomic nerves. Shimazu T, Nutrition 1996 12 65 66 8838845
13. SCN output drives the autonomic nervous system: with special reference to the autonomic function related to the regulation of glucose metabolism. Nagai K, Nagai N, Shimizu K, Chun S, Nakagawa H, Niijima A, Prog Brain Res 1996 111 253 272 8990920
14. Regulation of insulin secretion by nerves and neuropeptides. Ahren B, Ann Acad Med Singapore 1999 28 99 104 10374034
15. Decreased adrenal medullary catecholamine release in spontaneously diabetic BB-Wistar rats. Role of hypoglycemia. Wilke RA, Hillard CJ, Diabetes 1994 43 724 729 10.2337/diabetes.43.5.724 8168651
16. Mechanisms and physiological significance of the cholinergic control of pancreatic beta-cell function. Gilon P, Henquin JC, Endocr Rev 2001 22 565 604 10.1210/er.22.5.565 11588141
17. Neurogenic hypotension in patients with severe head injuries. Chesnut RM, Gautille T, Blunt BA, Klauber MR, Marshall LF, J Trauma 1998 44 958 963 discussion 963-954 10.1097/00005373-199806000-00003 9637149
18. Tyrosine hydroxylase-containing fibres extend from the rat corpus striatum into grafts of muscularis externa and myenteric plexus. Tew EM, Fearon A, Anderson PN, Burnstock G, Neurosci Lett 1995 194 33 36 10.1016/0304-3940(95) 11714-8 7478206
19. Autonomic regulation of islet hormone secretion-implications for health and disease. Ahren B, Diabetologia 2000 43 393 410 10.1007/s001250051322 10819232
20. An autonomic hypothesis for hypothalamic obesity. Inoue S, Bray GA, Life Sci 1979 25 561 566 10.1016/0024-3205(79)90549-6 388132
21. Neuroendocrine regulation of nutrient partitioning. Rohner-Jeanrenaud F, Ann N Y Acad Sci 1999 892 261 271 10.1111/j.1749-6632.1999.tb07800.x 10842667
22. Autonomic activity and glycemic homeostasis are maintained by precocious and low intensity training exercises in MSG-programmed obese mice. Scomparin DX, Gomes RM, Grassiolli S, Rinaldi W, Martins AG, de Oliveira JC, Gravena C, de Freitas Mathias PC, Endocrine 2009 36 510 517 10.1007/s12020-009-9263-2 19856134
23. Parasympathetic blockade attenuates augmented pancreatic polypeptide but not insulin secretion in Pima Indians. Vozarova De Courten B, Weyer C, Stefan N, Horton M, DelParigi A, Havel P, Bogardus C, Tataranni PA, Diabetes 2004 53 663 671 10.2337/diabetes.53.3.663 14988250
24. Decreased cholinergic stimulation of insulin secretion by islets from rats fed a low protein diet is associated with reduced protein kinase calpha expression. Ferreira F, Filiputti E, Arantes VC, Stoppiglia LF, Araujo EP, Delghingaro-Augusto V, Latorraca MQ, Toyama MH, Boschero AC, Carneiro EM, J Nutr 2003 133 695 699 12612139
25. Altered activity of the autonomous nervous system as a determinant of the impaired beta-cell secretory response after protein-energy restriction in the rat. Leon-Quinto T, Magnan C, Portha B, Endocrinology 1998 139 3382 3389 10.1210/en.139.8.3382 9681486
26. From physiology to neuroendocrinology: a reappraisal of risk factors of body weight gain in humans. Tataranni PA, Diabetes Metab 1998 24 108 115 9592634
27. The epidemiology of obesity: the size of the problem. James WP, J Intern Med 2008 263 336 352 10.1111/j.1365-2796.2008.01922.x 18312311
28. Who, when, and how much? Epidemiology of walking in a middle-income country. Hallal PC, Azevedo MR, Reichert FF, Siqueira FV, Araujo CL, Victora CG, Am J Prev Med 2005 28 156 161 10.1016/j.amepre.2004.10.012 15710270
29. Sympathetic hyperresponsiveness to hypothalamic stimulation in young hypertensive rats. Bunag RD, Takeda K, Am J Physiol 1979 237 39 R44 37744
30. Dual viral transneuronal tracing of central autonomic circuits involved in the innervation of the two kidneys in rat. Cano G, Card JP, Sved AF, J Comp Neurol 2004 471 462 481 10.1002/cne.20040 15022264
31. Programming by early nutrition: an experimental approach. Lucas A, J Nutr 1998 128 401S 406S 9478036
32. Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity. Heindel JJ, Vom Saal FS, Mol Cell Endocrinol 2009 304 90 96 10.1016/j.mce.2009.02.025 19433253
33. DNA methylation patterns and epigenetic memory. Bird A, Genes Dev 2002 16 6 21 10.1101/gad.947102 11782440
34. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? Burdge GC, Hanson MA, Slater-Jefferies JL, Lillycrop KA, Br J Nutr 2007 97 1036 1046 10.1017/S0007114507682920 17381976
35. Adverse effects of nutritional programming during prenatal and early postnatal life, some aspects of regulation and potential prevention and treatments. Guilloteau P, Zabielski R, Hammon HM, Metges CC, J Physiol Pharmacol 2009 60 Suppl 3 17 35 19996479
36. Early nutrition and epigenetic programming: chasing shadows. Attig L, Gabory A, Junien C, Curr Opin Clin Nutr Metab Care 2010 13 284 293 10.1097/MCO.0b013e328338aa61 20375884
37. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH, Proc Natl Acad Sci U S A 2008 105 17046 17049 10.1073/pnas.0806560105 18955703
38. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. Park JH, Stoffers DA, Nicholls RD, Simmons RA, J Clin Invest 2008 118 2316 2324 18464933
39. Early-life programming of susceptibility to dysregulation of glucose metabolism and the development of Type 2 diabetes mellitus. Holness MJ, Langdown ML, Sugden MC, Biochem J 2000 349 Pt 3 657 665 10903125
40. Beta-cell failure as a complication of diabetes. Chang-Chen KJ, Mullur R, Bernal-Mizrachi E, Rev Endocr Metab Disord 2008 9 329 343 10.1007/s11154-008- 9101-5 18777097
41. The developmental origins of chronic adult disease. Barker DJ, Acta Paediatr Suppl 2004 93 26 33 15702667
42. Long-term effects of early malnutrition on body weight regulation. Sawaya AL, Martins PA, Grillo LP, Florencio TT, Nutr Rev 2004 62 127 S133 15387478
43. The diabetic pregnancy, macrosomia, and perinatal nutritional programming. Plagemann A, Harder T, Dudenhausen JW, Nestle Nutr Workshop Ser Pediatr Program 2008 61 91 102 18196947
44. Chronic high-NaCl intake prolongs the cardiorenal responses to central N/OFQ and produces regional changes in the endogenous brain NOP receptor system. Wainford RD, Kapusta DR, Am J Physiol Regul Integr Comp Physiol 2009 296 280 R288 18987291
45. Activation of Rho-kinase in the brainstem enhances sympathetic drive in mice with heart failure. Ito K, Kimura Y, Hirooka Y, Sagara Y, Sunagawa K, Auton Neurosci 2008 142 77 81 10.1016/j.autneu.2008.07.010 18762460
46. Medullary pathways mediating the parasubthalamic nucleus depressor response. Ciriello J, Solano-Flores LP, Rosas-Arellano MP, Kirouac GJ, Babic T, Am J Physiol Regul Integr Comp Physiol 2008 294 1276 R1284 10.1152/ajpregu. 00437.2007 18287224
47. Growth failure and pituitary function in CHARGE and VATER associations. Khadilkar VV, Cameron FJ, Stanhope R, Arch Dis Child 1999 80 167 170 10.1136/adc.80.2.167 10325734
48. Role of the autonomic nervous system in the development of hyperinsulinemia by high-carbohydrate formula feeding to neonatal rats. Mitrani P, Srinivasan M, Dodds C, Patel MS, Am J Physiol Endocrinol Metab 2007 292 1069 E1078 17164433
49. Developmental origins of obesity: a sympathoadrenal perspective. Young JB, Int J Obes (Lond) 2006 30 Suppl 4 41 S49
50. Insulin secretion impairment and insulin sensitivity improvement in adult rats undernourished during early lactation. Moura AS, Caldeira Filho JS, de Freitas Mathias PC, de Sa CC, Res Commun Mol Pathol Pharmacol 1997 96 179 192 9226752
51. Evidence for impaired insulin production and higher sensitivity in stunted children living in slums. Martins PA, Sawaya AL, Br J Nutr 2006 95 996 1001 10.1079/BJN20061754 16611392
52. Blockade of the 32P phosphate flush of pancreatic beta cells from adult rats who received a low-protein diet during early lactation. Barbosa FB, Gravena C, Mathias P, Moura AS, Braz J Med Biol Res 1993 26 1355 1358 8136737
53. Protein restriction during lactation alters the autonomic nervous system control on glucose-induced insulin secretion in adult rats. Gravena C, Andreazzi AE, Mecabo FT, Grassiolli S, Scantamburlo VM, Mathias PC, Nutr Neurosci 2007 10 79 87 10.1080/10284150701308693 17539486
54. Acute effects of fatty acids on insulin secretion from rat and human islets of Langerhans. Gravena C, Mathias PC, Ashcroft SJ, J Endocrinol 2002 173 73 80 10.1677/joe.0.1730073 11927386
55. Programming of the endocrine pancreas by the early nutritional environment. Reusens B, Remacle C, Int J Biochem Cell Biol 2006 38 913 922 10.1016/j.biocel.2005.10.012 16337425
56. 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. Sebaai N, Lesage J, Breton C, Vieau D, Deloof S, Neuroendocrinology 2004 79 163 173 10.1159/000078098 15153750
57. Maternal perinatal undernutrition has long-term consequences on morphology, function and gene expression of the adrenal medulla in the adult male rat. Laborie C, Molendi-Coste O, Breton C, Montel V, Vandenbulcke F, Grumolato L, Anouar Y, Vieau D, J Neuroendocrinol 2011 23 711 724 10.1111/j.1365-2826.2011.02159.x 21564351
58. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD, Am J Physiol Endocrinol Metab 2000 279 83 E87 10893326
59. Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. Breton C, Lukaszewski MA, Risold PY, Enache M, Guillemot J, Riviere G, Delahaye F, Lesage J, Dutriez-Casteloot I, Laborie C, Vieau D, Am J Physiol Endocrinol Metab 2009 296 462 E472 19088253
60. Influence of early nutrition on growth and adipose tissue characteristics in male and female rats. Bassett DR, Craig BW, J Appl Physiol 1988 64 1249 1256 10.1063/1.342505 3284871
61. Sexual dimorphism in environmental epigenetic programming. Gabory A, Attig L, Junien C, Mol Cell Endocrinol 2009 304 8 18 10.1016/j.mce.2009.02.015 19433243
62. 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. Loizzo S, Vella S, Loizzo A, Fortuna A, Di Biase A, Salvati S, Frajese GV, Agrapart V, Ramirez Morales R, Spampinato S, et al. Peptides 2010 31 1598 1605 10.1016/j.peptides.2010.05.006 20493223
63. Association between nutrition and gender during lactation influencing glucose homeostasis and blood pressure of the adult offspring. Moura AS, Franco De Sa CC, Lopez Da Costa C, Vicente LL, Guerreiro SM, Pinto AM, Biol Neonate 2002 82 263 270 10.1159/000065889 12381935
64. Gender-specific programming of insulin secretion and action. Sugden MC, Holness MJ, J Endocrinol 2002 175 757 767 10.1677/joe.0.1750757 12475386
65. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN, Ozanne SE, Am J Physiol Regul Integr Comp Physiol 2005 288 368 R373 15514105
66. 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. Zambrano E, Bautista CJ, Deas M, Martinez-Samayoa PM, Gonzalez-Zamorano M, Ledesma H, Morales J, Larrea F, Nathanielsz PW, J Physiol 2006 571 221 230 16339179
67. 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. Zambrano E, Martinez-Samayoa PM, Bautista CJ, Deas M, Guillen L, Rodriguez-Gonzalez GL, Guzman C, Larrea F, Nathanielsz PW, J Physiol 2005 566 225 236 10.1113/jphysiol.2005.086462 15860532
68. The stimulus-secretion coupling of amino acid-induced insulin release: insulinotropic action of branched-chain amino acids at physiological concentrations of glucose and glutamine. Sener A, Malaisse WJ, Eur J Clin Invest 1981 11 455 460 10.1111/j.1365-2362.1981.tb02013.x 6800820
69. Association of NAD(P)H oxidase with glucose-induced insulin secretion by pancreatic beta-cells. Morgan D, Rebelato E, Abdulkader F, Graciano MF, Oliveira-Emilio HR, Hirata AE, Rocha MS, Bordin S, Curi R, Carpinelli AR, Endocrinology 2009 150 2197 2201 19147679
70. Effects of 2-ketoisocaproate on insulin release and single potassium channel activity in dispersed rat pancreatic beta-cells. Ashcroft FM, Ashcroft SJ, Harrison DE, J Physiol 1987 385 517 529 2443671
71. Genetic variations in the pancreatic ATP-sensitive potassium channel, beta-cell dysfunction, and susceptibility to type 2 diabetes. Chistiakov DA, Potapov VA, Khodirev DC, Shamkhalova MS, Shestakova MV, Nosikov VV, Acta Diabetol 2009 46 43 49 10.1007/s00592-008-0056-5 18758683
72. Triggering and amplifying pathways of regulation of insulin secretion by glucose. Henquin JC, Diabetes 2000 49 1751 1760 10.2337/diabetes.49.11.1751 11078440
73. Pancreatic islet insulin secretion and metabolism in adult rats malnourished during neonatal life. Barbosa FB, Capito K, Kofod H, Thams P, Br J Nutr 2002 87 147 155 10.1079/BJN2001489 11895167
74. Maternal protein malnutrition does not impair insulin secretion from pancreatic islets of offspring after transplantation into diabetic rats. Branco RC, de Oliveira JC, Grassiolli S, Miranda RA, Barella LF, Gomes RM, Bataglini LA, Torrezan R, Gravena C, de Freitas Mathias PC, PLoS One 2012 7 30685 10.1371/journal.pone.0030685 22383969
75. Neuropeptides and the regulation of islet function. Ahren B, Wierup N, Sundler F, Diabetes 2006 55 Suppl 2 98 S107
76. Muscarinic receptors-characterization, coupling and function. Caulfield MP, Pharmacol Ther 1993 58 319 379 10.1016/0163-7258(93)90027-B 7504306
77. Cloning and expression of the human and rat m5 muscarinic acetylcholine receptor genes. Bonner TI, Young AC, Brann MR, Buckley NJ, Neuron 1988 1 403 410 10.1016/0896-6273(88)90190-0 3272174
78. Muscarinic receptor subtypes mediate stimulatory and paradoxical inhibitory effects on an insulin-secreting beta cell line. Miguel JC, Abdel-Wahab YH, Mathias PC, Flatt PR, Biochim Biophys Acta 2002 1569 45 50 10.1016/S0304-4165(01)00232-X 11853956
79. Quantitative and functional characterization of muscarinic receptor subtypes in insulin-secreting cell lines and rat pancreatic islets. Iismaa TP, Kerr EA, Wilson JR, Carpenter L, Sims N, Biden TJ, Diabetes 2000 49 392 398 10.2337/diabetes.49.3.392 10868960
80. 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. Balakrishnan S, Mathew J, Antony S, Paulose CS, Eur J Pharmacol 2009 608 14 22 10.1016/j.ejphar.2009.01.047 19347982
81. Oxotremorine-m potentiation of glucose-induced insulin release from rat islets involves M3 muscarinic receptors. Boschero AC, Szpak-Glasman M, Carneiro EM, Bordin S, Paul I, Rojas E, Atwater I, Am J Physiol 1995 268 336 E342 7864111
82. Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Yamada M, Miyakawa T, Duttaroy A, Yamanaka A, Moriguchi T, Makita R, Ogawa M, Chou CJ, Xia B, Crawley JN, et al. Nature 2001 410 207 212 10.1038/35065604 11242080
83. Muscarinic stimulation of pancreatic insulin and glucagon release is abolished in m3 muscarinic acetylcholine receptor-deficient mice. Duttaroy A, Zimliki CL, Gautam D, Cui Y, Mears D, Wess J, Diabetes 2004 53 1714 1720 10.2337/diabetes.53.7.1714 15220195
84. Beneficial metabolic effects caused by persistent activation of beta-cell M3 muscarinic acetylcholine receptors in transgenic mice. Gautam D, Ruiz De Azua I, Li JH, Guettier JM, Heard T, Cui Y, Lu H, Jou W, Gavrilova O, Zawalich WS, Wess J, Endocrinology 2010 151 5185 5194 10.1210/en.2010-0519 20843999
85. Maternal low-protein diet during lactation programmes body composition and glucose homeostasis in the adult rat offspring. Fagundes AT, Moura EG, Passos MC, Oliveira E, Toste FP, Bonomo IT, Trevenzoli IH, Garcia RM, Lisboa PC, Br J Nutr 2007 98 922 928 17524178
86. GABAergic basal forebrain neurons project to the neocortex: the localization of glutamic acid decarboxylase and choline acetyltransferase in feline corticopetal neurons. Fisher RS, Buchwald NA, Hull CD, Levine MS, J Comp Neurol 1988 272 489 502 10.1002/cne.902720404 2843581
87. Development of the neuroendocrine hypothalamus. Markakis EA, Front Neuroendocrinol 2002 23 257 291 10.1016/S0091-3022(02)00003-1 12127306