Publication Cover
Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 23, 2020 - Issue 6
235
Views
12
CrossRef citations to date
0
Altmetric
Articles

Malnutrition during late pregnancy exacerbates high-fat-diet-induced metabolic dysfunction associated with lower sympathetic nerve tonus in adult rat offspring

, , , , , , , , , , , , , , & ORCID Icon show all

References

  • Hruby A, Hu FB. The epidemiology of obesity: a big picture. Pharmacoeconomics 2015;33:673–89. doi: 10.1007/s40273-014-0243-x
  • Uauy R, Albala C, Kain J. Obesity trends in Latin America: transiting from under- to overweight. J Nutr 2001;131:893S–899S. doi: 10.1093/jn/131.3.893S
  • Lucas A. Programming not metabolic imprinting. Am J Clin Nutr 2000;71:602. doi: 10.1093/ajcn/71.2.602
  • Levin BE. Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos Trans R Soc Lond B Biol Sci 2006;361:1107–121. doi: 10.1098/rstb.2006.1851
  • Langley-Evans SC, Bellinger L, McMullen S. Animal models of programming: early life influences on appetite and feeding behaviour. Matern Child Nutr 2005;1:142–8. doi: 10.1111/j.1740-8709.2005.00015.x
  • Ravelli GP, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 1976;295: 349–53. doi: 10.1056/NEJM197608122950701
  • 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:E83–7. doi: 10.1152/ajpendo.2000.279.1.E83
  • Zubiria MG, Alzamendi A, Moreno G, Rey MA, Spinedi E, Giovambattista A. Long-term fructose intake increases adipogenic potential: evidence of direct effects of fructose on adipocyte precursor cells. Nutrients 2016;8:198. doi: 10.3390/nu8040198
  • Rask-Madsen C, Kahn CR. Tissue-specific insulin signaling, metabolic syndrome, and cardiovascular disease. Arterioscler Thromb Vasc Biol 2012;32:2052–9. doi: 10.1161/ATVBAHA.111.241919
  • de Oliveira JC, Grassiolli S, Gravena C, de Mathias PC. Early postnatal low-protein nutrition, metabolic programming and the autonomic nervous system in adult life. Nutr Metab (Lond) 2012;9:80. doi: 10.1186/1743-7075-9-80
  • Bertin E, Gangnerau MN, Bailbe D, Portha B. Glucose metabolism and beta-cell mass in adult offspring of rats protein and/or energy restricted during the last week of pregnancy. Am J Physiol 1999;277:E11–7.
  • Woodall SM, Breier BH, Johnston BM, Gluckman PD. A model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: effects on the somatotrophic axis and postnatal growth. J Endocrinol 1996;150:231–42. doi: 10.1677/joe.0.1500231
  • Franco Mdo C, Arruda RM, Fortes ZB, de Oliveira SF, Carvalho MH, Tostes RC, et al. Severe nutritional restriction in pregnant rats aggravates hypertension, altered vascular reactivity, and renal development in spontaneously hypertensive rats offspring. J Cardiovasc Pharmacol 2002;39:369–77. doi: 10.1097/00005344-200203000-00008
  • Han R, Li A, Li L, Kitlinska JB, Zukowska Z. Maternal low-protein diet up-regulates the neuropeptide Y system in visceral fat and leads to abdominal obesity and glucose intolerance in a sex- and time-specific manner. FASEB J 2012;26:3528–36. doi: 10.1096/fj.12-203943
  • Buettner R, Scholmerich J, Bollheimer LC. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 2007;15:798–808. doi: 10.1038/oby.2007.608
  • Barella LF, Miranda RA, Franco CC, Alves VS, Malta A, Ribeiro TA, et al. Vagus nerve contributes to metabolic syndrome in high-fat diet-fed young and adult rats. Exp Physiol 2015;100:57–68. doi: 10.1113/expphysiol.2014.082982
  • Barella LF, de Oliveira JC, Branco RC, Camargo RL, Gomes RM, Mendes FC, et al. Early exposure to a high-fat diet has more drastic consequences on metabolism compared with exposure during adulthood in rats. Horm Metab Res 2012;44:458–64. doi: 10.1055/s-0032-1306300
  • de Oliveira JC, Lisboa PC, de Moura EG, Barella LF, Miranda RA, Malta A, et al. Poor pubertal protein nutrition disturbs glucose-induced insulin secretion process in pancreatic islets and programs rats in adulthood to increase fat accumulation. J Endocrinol 2013;216:195–206. doi: 10.1530/JOE-12-0408
  • Druet C, Stettler N, Sharp S, Simmons RK, Cooper C, Smith GD, et al. Prediction of childhood obesity by infancy weight gain: an individual-level meta-analysis. Paediatr Perinat Epidemiol 2012;26:19–26. doi: 10.1111/j.1365-3016.2011.01213.x
  • de Oliveira JC, Scomparin DX, Andreazzi AE, Branco RC, Martins AG, Gravena C, et al. Metabolic imprinting by maternal protein malnourishment impairs vagal activity in adult rats. J Neuroendocrinol 2011;23:148–57. doi: 10.1111/j.1365-2826.2010.02095.x
  • Reeves PG, Nielsen FH, Fahey GC, Jr. 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-76A rodent diet. J Nutr 1993;123:1939–51. doi: 10.1093/jn/123.11.1939
  • Aref AB, Ahmed OM, Ali LA, Semmler M. Maternal rat diabetes mellitus deleteriously affects insulin sensitivity and beta-cell function in the offspring. J Diabetes Res 2013;2013:429154. doi: 10.1155/2013/429154
  • Trinder P. Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen. J Clin Pathol 1969;22:158–61. doi: 10.1136/jcp.22.2.158
  • Scott AM, Atwater I, Rojas E. A method for the simultaneous measurement of insulin release and B cell membrane potential in single mouse islets of Langerhans. Diabetologia 1981;21:470–5. doi: 10.1007/BF00257788
  • Malta A, de Moura EG, Ribeiro TA, Tofolo LP, Abdennebi-Najar L, Vieau D, et al. Protein-energy malnutrition at mid-adulthood does not imprint long-term metabolic consequences in male rats. Eur J Nutr 2016;55:1423–33. doi: 10.1007/s00394-015-0960-8
  • de Oliveira JC, Gomes RM, Miranda RA, Barella LF, Malta A, Martins IP, et al. Protein restriction during the last third of pregnancy malprograms the neuroendocrine axes to induce metabolic syndrome in adult male rat offspring. Endocrinology 2016;157:1799–812. doi: 10.1210/en.2015-1883
  • Milanski M, Arruda AP, Coope A, Ignacio-Souza LM, Nunez CE, Roman EA, et al. Inhibition of hypothalamic inflammation reverses diet-induced insulin resistance in the liver. Diabetes 2012;61:1455–62. doi: 10.2337/db11-0390
  • Pacini G, Mari A. Methods for clinical assessment of insulin sensitivity and beta-cell function. Best Pract Res Clin Endocrinol Metab 2003;17:305–22. doi: 10.1016/S1521-690X(03)00042-3
  • FagundesAT, Moura EG, Passos MC, Santos-Silva AP, de Oliveira E, Trevenzoli IH, et al. Temporal evaluation of body composition, glucose homeostasis and lipid profile of male rats programmed by maternal protein restriction during lactation. Horm Metab Res 2009;41:866–73. doi: 10.1055/s-0029-1233457
  • 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. doi: 10.1677/joe.0.1730073
  • Rinaldi W, Gomes RM, Scomparin DX, Grassiolli S, Ribeiro TA, Fabricio GS, et al. Low-intensity and moderate exercise training improves autonomic nervous system activity imbalanced by postnatal early overfeeding in rats. J Int Soc Sports Nutr 2014;11:25. doi: 10.1186/1550-2783-11-25
  • Sata F. [Developmental origins of health and disease (DOHaD) and epidemiology]. Nihon Eiseigaku Zasshi 2016;71:41–6. doi: 10.1265/jjh.71.41
  • Barker DJ. The fetal and infant origins of disease. Eur J Clin Invest 1995;25:457–63. doi: 10.1111/j.1365-2362.1995.tb01730.x
  • Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 1999;70:811–6. doi: 10.1093/ajcn/70.5.811
  • Thompson NM, Norman AM, Donkin SS, Shankar RR, Vickers MH, Miles JL, et al. Prenatal and postnatal pathways to obesity: different underlying mechanisms, different metabolic outcomes. Endocrinology 2007;148:2345–54. doi: 10.1210/en.2006-1641
  • Lukaszewski MA, Mayeur S, Fajardy I, Delahaye F, Dutriez-Casteloot I, Montel V, et al. Maternal prenatal undernutrition programs adipose tissue gene expression in adult male rat offspring under high-fat diet. Am J Physiol Endocrinol Metab 2011;301:E548–59. doi: 10.1152/ajpendo.00011.2011
  • Jones AP, Friedman MI. Obesity and adipocyte abnormalities in offspring of rats undernourished during pregnancy. Science 1982;215:1518–9. doi: 10.1126/science.7063860
  • Gauguier D, Bihoreau MT, Picon L, Ktorza A. Insulin secretion in adult rats after intrauterine exposure to mild hyperglycemia during late gestation. Diabetes 1991;40(Suppl 2):109–14. doi: 10.2337/diab.40.2.S109
  • Jaquet D, Deghmoun S, Chevenne D, Collin D, Czernichow P, Levy-Marchal C. Dynamic change in adiposity from fetal to postnatal life is involved in the metabolic syndrome associated with reduced fetal growth. Diabetologia 2005;48:849–55. doi: 10.1007/s00125-005-1724-4
  • Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993;36:62–7. doi: 10.1007/BF00399095
  • Ozanne SE, Hales CN. Lifespan: catch-up growth and obesity in male mice. Nature 2004;427:411–2. doi: 10.1038/427411b
  • Vickers MH, Ikenasio BA, Breier BH. IGF-I treatment reduces hyperphagia, obesity, and hypertension in metabolic disorders induced by fetal programming. Endocrinology 2001;142:3964–73. doi: 10.1210/endo.142.9.8390
  • Desai M, Gayle D, Han G, Ross MG. Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reprod Sci 2007;14:329–37. doi: 10.1177/1933719107303983
  • Coupe B, Dutriez-Casteloot I, Breton C, Lefevre F, Mairesse J, Dickes-Coopman A, et al. Perinatal undernutrition modifies cell proliferation and brain-derived neurotrophic factor levels during critical time-windows for hypothalamic and hippocampal development in the male rat. J Neuroendocrinol 2009;21:40–8. doi: 10.1111/j.1365-2826.2008.01806.x
  • Erhuma A, Bellinger L, Langley-Evans SC, Bennett AJ. Prenatal exposure to undernutrition and programming of responses to high-fat feeding in the rat. Br J Nutr 2007;98:517–24. doi: 10.1017/S0007114507721505
  • Nielsen MO, Kongsted AH, Thygesen MP, Strathe AB, Caddy S, Quistorff B, et al. Late gestation undernutrition can predispose for visceral adiposity by altering fat distribution patterns and increasing the preference for a high-fat diet in early postnatal life. Br J Nutr 2013;109:2098–110. doi: 10.1017/S0007114512004199
  • Muhlhausler B, Smith SR. Early-life origins of metabolic dysfunction: role of the adipocyte. Trends Endocrinol Metab 2009;20:51–7. doi: 10.1016/j.tem.2008.10.006
  • O'Dowd JF, Stocker CJ. Endocrine pancreatic development: impact of obesity and diet. Front Physiol 2013;4:170. doi: 10.3389/fphys.2013.00170
  • Grayson BE, Allen SE, Billes SK, Williams SM, Smith MS, Grove KL. Prenatal development of hypothalamic neuropeptide systems in the nonhuman primate. Neuroscience 2006;143:975–86. doi: 10.1016/j.neuroscience.2006.08.055
  • Garofano A, Czernichow P, Breant B. In utero undernutrition impairs rat beta-cell development. Diabetologia 1997;40:1231–4. doi: 10.1007/s001250050812
  • Desai M, Guang H, Ferelli M, Kallichanda N, Lane RH. Programmed upregulation of adipogenic transcription factors in intrauterine growth-restricted offspring. Reprod Sci 2008;15:785–96. doi: 10.1177/1933719108318597
  • Ikenasio-Thorpe BA, Breier BH, Vickers MH, Fraser M. Prenatal influences on susceptibility to diet-induced obesity are mediated by altered neuroendocrine gene expression. J Endocrinol 2007;193:31–7. doi: 10.1677/joe.1.07017
  • Teff KL. Visceral nerves: vagal and sympathetic innervation. JPEN J Parenter Enteral Nutr 2008;32:569–71. doi: 10.1177/0148607108321705
  • Bartness TJ, Bamshad M. Innervation of mammalian white adipose tissue: implications for the regulation of total body fat. Am J Physiol 1998;275:R1399–411.
  • Bray GA. Reciprocal relation between the sympathetic nervous system and food intake. Brain Res Bull 1991;27:517–20. doi: 10.1016/0361-9230(91)90152-A
  • Garcia AP, Palou M, Sanchez J, Priego T, Palou A, Pico C. Moderate caloric restriction during gestation in rats alters adipose tissue sympathetic innervation and later adiposity in offspring. PLoS One 2011;6:e17313. doi: 10.1371/journal.pone.0017313
  • Tonkiss J, Galler, J, Morgane, PJ, Bronzino, JD, Austin-LaFrance, RJ. Prenatal protein malnutrition and postnatal brain function. Ann N Y Acad Sci 1993;678:215–27. doi: 10.1111/j.1749-6632.1993.tb26124.x
  • Plagemann A, Harder T, Rake A, Melchior K, Rohde W, Dorner G. Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr 2000;130:2582–9. doi: 10.1093/jn/130.10.2582
  • Vander Tuig JG, Knehans AW, Romsos DR. Reduced sympathetic nervous system activity in rats with ventromedial hypothalamic lesions. Life Sci 1982;30:913–20. doi: 10.1016/0024-3205(82)90619-1
  • Vozarova de Courten B, Weyer C, Stefan N, Horton M, DelParigi A, Havel P, et al. Parasympathetic blockade attenuates augmented pancreatic polypeptide but not insulin secretion in Pima Indians. Diabetes 2004;53:663–71. doi: 10.2337/diabetes.53.3.663

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.