Short-and long-term effects of maternal perinatal undernutrition are lowered by cross-fostering during lactation in the male rat

Journal of Developmental Origins of Health and Disease

Volumn 5, Issue 2, 2014, Pages 109-120

  Wattez, J S ^a   Delahaye, F ^a,b   Barella, L F ^c   Dickes Coopman, A ^a   Montel, V ^a   Breton, C ^a   Mathias, P ^c   Foligne B ^d,e   Lesage, J ^a   Vieau, D ^a  

^a UNIV LILLE   (France)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c STATE UNIVERSITY OF MARINGÁ   (Brazil)

^d INSERM U1019   (France)

^e INSERM   (France)

Author keywords

cross fostering; DOHaD; lactation; leptin; undernutrition

Indexed keywords

ALDOSTERONE; ATRIAL NATRIURETIC FACTOR; GLUCOSE; LEPTIN; VASOPRESSIN DERIVATIVE;

ANIMAL; BLOOD; BLOOD PRESSURE; BODY COMPOSITION; COMPLICATION; FEMALE; HEART RATE; LACTATION; MALE; MALNUTRITION; MATERNAL NUTRITION; METABOLISM; NEWBORN; PREGNANCY; TIME; WISTAR RAT;

ALDOSTERONE; ANIMALS; ANIMALS, NEWBORN; ATRIAL NATRIURETIC FACTOR; BLOOD PRESSURE; BODY COMPOSITION; FEMALE; GLUCOSE; HEART RATE; LACTATION; LEPTIN; MALE; MALNUTRITION; PREGNANCY; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; RATS, WISTAR; TIME FACTORS; VASOPRESSINS;

EID: 84902169232     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174413000548     Document Type: Article

References (62)

1. Barker DJP. The developmental origins of chronic adult disease. Acta Paediatr Suppl. 2004; 93, 26-33.
2. Gluckman PD, Hanson MA, Spencer HG, Bateson P. Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc R Soc B Biol Sci. 2005; 272, 671-677.
3. Levin BE. Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos Trans R Soc B Biol Sci. 2006; 361, 1107-1121.
4. Langley-Evans SC. Developmental programming of health and disease. Proc Nutr Soc. 2006; 65, 97-105.
5. Hales CN. Metabolic consequences of intrauterine growth retardation. Acta Paediatr Suppl. 1997; 423, 184-187.
6. Holemans K, Aerts L, Assche FAV. Fetal growth restriction and consequences for the offspring in animal models. J Soc Gynecol Investig. 2003; 10, 392-399.
7. Plagemann A, Harder T, Rake A, et al. Perinatal elevation of hypothalamic insulin, acquired malformation of hypothalamic galaninergic neurons, and syndrome x-like alterations in adulthood of neonatally overfed rats. Brain Res. 1999; 836, 146-155.
8. Habbout A, Li N, Rochette L, Vergely C. Postnatal overfeeding in rodents by litter size reduction induces major short-and long-term pathophysiological consequences. J Nutr. 2013; 143, 553-562.
9. Habbout A, Guenancia C, Lorin J, et al. Postnatal overfeeding causes early shifts in gene expression in the heart and long-term alterations in cardiometabolic and oxidative parameters. PLoS One. 2013; 8, e56981.
10. Bieswal F, Ahn M-T, Reusens B, et al. The importance of catchup growth after early malnutrition for the programming of obesity in male rat. Obes Silver Spring Md. 2006; 14, 1330-1343.
11. Lesage J, Blondeau B, Grino M, et al. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology. 2001; 142, 1692-1702.
12. Delahaye F, Breton C, Risold P-Y, et al. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology. 2007; 149, 470-475.
13. Sebaai N, Lesage J, Alaoui A, et al. Effects of dehydration on endocrine regulation of the electrolyte and fluid balance and atrial natriuretic peptide-binding sites in perinatally malnourished adult male rats. Eur J Endocrinol Eur Fed Endocr Soc. 2002; 147, 835-848.
14. Vieau D, Sebaai N, Léonhardt M, et al. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology. 2007; 32(Suppl. 1), S16-S20.
15. Laborie C, Molendi-Coste O, Breton C, et al. 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.
16. Léonhardt M, Lesage J, Croix D, et al. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod. 2003; 68, 390-400.
17. Singhal A, Fewtrell M, Cole TJ, Lucas A. Low nutrient intake and early growth for later insulin resistance in adolescents born preterm. Lancet. 2003; 361, 1089-1097.
18. Eriksson JG, Forsen T, Tuomilehto J, et al. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ. 1999; 318, 427-431.
19. Ong KKL. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000; 320, 967-971.
20. Ravelli AC, van der Meulen JH, Osmond C, et al. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr. 1999; 70, 811-816.
21. Kristensen P, Judge ME, Thim L, et al. Hypothalamic CART is a new anorectic peptide regulated by leptin. Nature. 1998; 393, 72-76.
22. Elias CF, Lee C, Kelly J, et al. Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron. 1998; 21, 1375-1385.
23. Hahn TM, Breininger JF, Baskin DG, Schwartz MW. Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat Neurosci. 1998; 1, 271-272.
24. Broberger C, Johansen J, Johansson C, et al. The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc Natl Acad Sci. 1998; 95, 15043-15048.
25. Kieffer TJ, Habener JF. The adipoinsular axis: effects of leptin on pancreatic beta-cells. Am J Physiol Endocrinol Metab. 2000; 278, E1-E14.
26. Ahima RS, Prabakaran D, Flier JS. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest. 1998; 101, 1020-1027.
27. Bouret SG, Draper SJ, Simerly RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004; 304, 108-110.
28. Vickers MH, Gluckman PD, Coveny AH, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005; 146, 4211-4216.
29. Léonhardt M, Lesage J, Dufourny L, et al. Perinatal maternal food restriction induces alterations in hypothalamo-pituitary-adrenal axis activity and in plasma corticosterone-binding globulin capacity of weaning rat pups. Neuroendocrinology. 2002; 75, 45-54.
30. Delahaye F, Lukaszewski M-A, Wattez J-S, et al. Maternal perinatal undernutrition programs a "brown-like" phenotype of gonadal white fat in male rat at weaning. AJP Regul Integr Comp Physiol. 2010; 299, R101-R110.
31. Sebaai N, Lesage J, Breton C, et al. 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.
32. Rivière G, Michaud A, Breton C, et al. Angiotensin-converting enzyme 2 (ACE2) and ACE activities display tissue-specific sensitivity to undernutrition-programmed hypertension in the adult rat. Hypertension. 2005; 46, 1169-1174.
33. VickersMH, Breier BH,CutfieldWS, 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.
34. Breton C, Lukaszewski M-A, Risold P-Y, et al. Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. AJP Endocrinol Metab. 2008; 296, E462-E472.
35. Lukaszewski M-A, Mayeur S, Fajardy I, et al. Maternal prenatal undernutrition programs adipose tissue gene expression in adult male rat offspring under high-fat diet. AJP Endocrinol Metab. 2011; 301, E548-E559.
36. Nicholls DG, Locke RM. Thermogenic mechanisms in brown fat. Physiol Rev. 1984; 64, 1-64.
37. Molendi-Coste O, Grumolato L, Laborie C, et al. Maternal perinatal undernutrition alters neuronal and neuroendocrine differentiation in the rat adrenal medulla at weaning. Endocrinology. 2006; 147, 3050-3059.
38. Garofano A, Czernichow P, Bréant B. Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia. 1999; 42, 711-718.
39. Branco RCS, de Oliveira JC, Grassiolli S, et al. Maternal protein malnutrition does not impair insulin secretion from pancreatic islets of offspring after transplantation into diabetic rats. PLoS One. 2012; 7, e30685.
40. Lesage J, Del-Favero F, Leonhardt M, et al. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J Endocrinol. 2004; 181, 291-296.
41. Venu L, Harishankar N, Krishna TP, Raghunath M. Does maternal dietary mineral restriction per se predispose the offspring to insulin resistance Eur J Endocrinol Eur Fed Endocr Soc. 2004; 151, 287-294.
42. Coupé B, Grit I, Hulin P, et al. Postnatal growth after intrauterine growth restriction alters central leptin signal and energy homeostasis. PLoS One. 2012; 7, e30616.
43. Desai M, Gayle D, Babu J, Ross MG. The timing of nutrient restriction during rat pregnancy/lactation alters metabolic syndrome phenotype. Am J Obstet Gynecol. 2007; 196, 555.e1-555.e7.
44. Mcmillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005; 85, 571-633.
45. Fagundes ATS, Moura EG, Passos MCF, 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, 866-873.
46. Lim JS, Lee JA, Hwang JS, et al. Non-catch-up growth in intrauterine growth-retarded rats showed glucose intolerance and increased expression of PDX-1 mRNA. Pediatr Int. 2011; 53, 181-186.
47. Howie GJ, Sloboda DM, Vickers MH. Maternal undernutrition during critical windows of development results in differential and sex-specific effects on postnatal adiposity and related metabolic profiles in adult rat offspring. Br J Nutr. 2012; 108, 298-307.
48. Lee S, Lee KA, Choi GY, et al. Feed restriction during pregnancy/lactation induces programmed changes in lipid, adiponectin and leptin levels with gender differences in rat offspring. J Matern Fetal Neonatal Med. 2013; 26, 908-914.
49. Alexandre-Gouabau M-CF, Bailly E, Moyon TL, et al. Postnatal growth velocity modulates alterations of proteins involved in metabolism and neuronal plasticity in neonatal hypothalamus in rats born with intrauterine growth restriction. J Nutr Biochem. 2012; 23, 140-152.
50. Lima Nda S, de Moura EG, Passos MCF, et al. Early weaning causes undernutrition for a short period and programmes some metabolic syndrome components and leptin resistance in adult rat offspring. Br J Nutr. 2011; 105, 1405-1413.
51. Matthews PA, Samuelsson A-M, Seed P, et al. Fostering in mice induces cardiovascular and metabolic dysfunction in adulthood. J Physiol. 2011; 589, 3969-3981.
52. Ellis-Hutchings RG, Zucker RM, Grey BE, et al. Altered health outcomes in adult offspring of Sprague Dawley and Wistar rats undernourished during early or late pregnancy. Birth Defects Res B Dev Reprod Toxicol. 2010; 89, 396-407.
53. Chamson-Reig A, Thyssen SM, Hill DJ, Arany E. Exposure of the pregnant rat to low protein diet causes impaired glucose homeostasis in the young adult offspring by different mechanisms in males and females. Exp Biol Med. 2009; 234, 1425-1436.
54. Gosby AK, Maloney CA, Caterson ID. Elevated insulin sensitivity in low-protein offspring rats is prevented by a high-fat diet and is associated with visceral fat. Obes Silver Spring Md. 2010; 18, 1593-1600.
55. Picó C, Oliver P, Sánchez J, et al. The intake of physiological doses of leptin during lactation in rats prevents obesity in later life. Int J Obes. 2007; 31, 1199-1209.
56. Stocker CJ, Wargent E, O'Dowd J, et al. Prevention of dietinduced obesity and impaired glucose tolerance in rats following administration of leptin to their mothers. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R1810-R1818.
57. Toste FP, deMoura EG, Lisboa PC, et al. Neonatal leptin treatment programmes leptin hypothalamic resistance and intermediary metabolic parameters in adult rat. Br J Nutr. 2007; 95, 830.
58. Patterson CM, Bouret SG, Park S, et al. Large litter rearing enhances leptin sensitivity and protects selectively bred dietinduced obese rats from becoming obese. Endocrinology. 2010; 151, 4270-4279.
59. Attig L, Solomon G, Ferezou J, et al. Early postnatal leptin blockage leads to a long-term leptin resistance and susceptibility to diet-induced obesity in rats. Int J Obes. 2008; 32, 1153-1160.
60. Casabiell X, Piñeiro V, Tomé MA, et al. Presence of leptin in colostrum and/or breast milk from lactating mothers: a potential role in the regulation of neonatal food intake. J Clin Endocrinol Metab. 1997; 82, 4270-4273.
61. Peleg-Raibstein D, Luca E, Wolfrum C. Maternal high-fat diet in mice programs emotional behavior in adulthood. Behav Brain Res. 2012; 233, 398-404.
62. Attig L, Brisard D, Larcher T, et al. Postnatal leptin promotes organ maturation and development in IUGR piglets. PLoS One. 2013; 8, e64616.