Skip to main content
SpringerLink
Log in

Neonatal Programming of Body Weight Regulation and Energetic Metabolism

  • Published:
Bioscience Reports

Programming is an epigenetic phenomena by which nutritional, hormonal, physical psychological and other stressful events acting in a critical period of life, such as gestation and lactation, modifies in a prolonged way certain physiological functions. This process was preserved by natural selection as an important adaptive tool for survival of organisms living in nutritional impaired areas. So, malnutrition during gestation and lactation turns on different genes that provide the organism with a thrifty phenotype. In the case of an abundant supply of nutrients after this period, those organisms that were adapted to a low metabolic waste and higher energy utilization will be in a higher risk of developing metabolic diseases, such as obesity, hyperlipidemia, diabetes mellitus and hypertension. The kind of malnutrition, duration and intensity are important for the type of programming obtained. We discuss some of the hormonal and metabolic changes that occur in gestation or lactation, when malnutrition is applied to the mothers and their offspring. Some of these changes, such as an increase of maternal triiodothyronine (T3), leptin and glucocorticoids (GC) and decrease in prolactin are by itself potential programming factors. Most of these hormones can be transfer through the milk that has other important macronutrients composition changes in malnourished dams. We discuss the programming effects of some of these hormones upon body weight and composition, leptin, thyroid and adrenal functions, and their effects on liver, muscle and adipose tissue metabolism and the consequences on thermogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • R. S. Ahima C. B. Saper J. S. Flyer J. K. Elmquist (2000) ArticleTitleLeptin regulation of neuroendocrine systems Front. Neuroendocrinol. 20 317–363

    Google Scholar 

  • K. Albertsson-Wikland M. Boguszewski J. Karlberg (1998) ArticleTitleChildren born small-for-gestational age: postnatal growth and hormonal status Hormone Res. 49 7–13 Occurrence Handle10.1159/000053080

    Article  Google Scholar 

  • R. M. Anguita D. M. Sigulem A. L. Sawaya (1993) ArticleTitleIntrauterine food restriction is associated with obesity in young rats J. Nutr. 123 1421–1428 Occurrence Handle8336213

    PubMed  Google Scholar 

  • A. Bado S. Levasseur S. Attoub S. Kermongant J. P. Laigneau M. N. Bortoluzzi L. Moizo T. Lehy N. Guerre-Millo Y. Le Marchand-Brustel M. J Lewin (1998) ArticleTitleThe stomach is a source of leptin Nature 394 790–793 Occurrence Handle10.1038/29547 Occurrence Handle9723619

    Article  PubMed  Google Scholar 

  • J. M. Bakker F. Bel ParticleVan C. J. Heijnen (2001) ArticleTitleNeonatal glucocorticoids and the developing brain: short-term treatment with life-long consequences? Trends Neurosci. 24 649–653 Occurrence Handle10.1016/S0166-2236(00)01948-2 Occurrence Handle11672809

    Article  PubMed  Google Scholar 

  • W. A. Banks A. J. Katin W. Huang J. B. Jaspan L. M. Mannes (1996) ArticleTitleLeptin enters the brain by a saturable system independent of insulin Peptides 17 305–311 Occurrence Handle10.1016/0196-9781(96)00025-3 Occurrence Handle8801538

    Article  PubMed  Google Scholar 

  • D. J. P. Barker C. N. Hales C. H. Fall C. Osmond K. Phipps P. M. Clark (1993) ArticleTitleType 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome x): relation to reduced fetal growth Diabetologia 36 62–67 Occurrence Handle10.1007/BF00399095 Occurrence Handle8436255

    Article  PubMed  Google Scholar 

  • P. C. Barrradas A. S. Ferraz A. A. Ferreira R. P. Daumas E. G. Moura (2000) ArticleTitle2′3′ cyclic nucleotide 3′phosphodiesterase immunohistochemistry shows an impairment on myelin compaction in hypothyroid rats Int. J. Dev. Neurosci. 18 887–892 Occurrence Handle10.1016/S0736-5748(00)00028-9 Occurrence Handle11154857

    Article  PubMed  Google Scholar 

  • E. Bertin M. N. Gangnerau D. Bailb’e B. Portha (1999) ArticleTitleGlucose metabolism and beta-cell mass in adult offspring of rats protein and/or energy restricted during the last week of pregnancy Am. J. Physiol. 277 E11–E17 Occurrence Handle10409122

    PubMed  Google Scholar 

  • C. Bertram A. R. Trowern N. Copin A. A. Jackson C. B. Whorwood (2001) ArticleTitleThe maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11_-hydroxysteroid dehydrogenase: potential molecular mechanisms underlying the programming of hypertension in utero Endocrinology 142 2841–2853 Occurrence Handle10.1210/en.142.7.2841 Occurrence Handle11416003

    Article  PubMed  Google Scholar 

  • C. Bjorbaek J. K. Elmquist J. D. Frantz S. E. Shoelson J. S. Flier (1998) ArticleTitleIdentification of SOCS-3 as a potential mediator of central leptin resistance Mol. Cell 16 19–25

    Google Scholar 

  • P. Bjorntorp R. Rosmond (2000) ArticleTitleObesity and Cortisol Nutrition 16 924–936 Occurrence Handle10.1016/S0899-9007(00)00422-6 Occurrence Handle11054598

    Article  PubMed  Google Scholar 

  • S. Bo P. Cavallo-Perin L. Scaglione G. Ciccone G. Pagano (2000) ArticleTitleLow birthweight and metabolic abnormalities in twins with increased susceptibility to type 2 diabetes Diabetic Med. 17 365–370 Occurrence Handle10.1046/j.1464-5491.2000.00288.x Occurrence Handle10872535

    Article  PubMed  Google Scholar 

  • M. C. S. Boguszewski G. Johannsson L. C. Fortes Y. B. Sverrisdóttir (2004) ArticleTitleLow birth size and final height predict high sympathetic nerve activity in adulthood J. Hypertens. 22 1157–1163 Occurrence Handle10.1097/00004872-200406000-00017 Occurrence Handle15167451

    Article  PubMed  Google Scholar 

  • S. G. Bouret S. J. Draper R. B. Simerly (2004a) ArticleTitleTrophic action of leptin on hypothalamic neurons that regulate feeding Science 304 108–115 Occurrence Handle10.1126/science.1095004

    Article  Google Scholar 

  • S. G. Bouret S. J. Draper R. B. Simerly (2004b) ArticleTitleFormation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice J. Neurosci. 24 2797–2805 Occurrence Handle10.1523/JNEUROSCI.5369-03.2004

    Article  Google Scholar 

  • B. H. Breier M. H. Vickers B. A. Ikenasio K. Y. Chan W. P. S. Wong (2001) ArticleTitleFetal programming of appetite and obesity Mol. Cell. Endocrinol. 185 73–79 Occurrence Handle10.1016/S0303-7207(01)00634-7 Occurrence Handle11738796

    Article  PubMed  Google Scholar 

  • S. P. Burns M. Desai R. D. Cohen C. N. Hales R. A. lles J. P. Germain T. C. Going R. A. Bailey (1997) ArticleTitleGluconeogenesis, glucose handling, and structural changes in livers of the adult offspring of rats partially deprived of protein during pregnancy and lactation J. Clin. Invest. 100 1768–1774 Occurrence Handle9312176

    PubMed  Google Scholar 

  • X. Casabiell V. Piñeiro M. A. Tomé R. Peinó C. Diéguez F. F. Casanueva (1997) ArticleTitlePresence of leptin in colostrum and/or breast milk from lactating mothers: a potencial role in the regulation of neonatal food intake J. Clin. Endocr. Metab. 82 4270–3 Occurrence Handle10.1210/jc.82.12.4270 Occurrence Handle9398752

    Article  PubMed  Google Scholar 

  • S. C. Chua SuffixJr. W. K. Chung X. S. Wu-Peng Y. Zhang S. M. Liu L. Tartaglia R. L. Leibel (1996) ArticleTitlePhenotypes of mouse diabetes and rat fatty due to mutations in the OB (leptin) receptor Science 271 994–996 Occurrence Handle8584938

    PubMed  Google Scholar 

  • S. Chan M. D. Kilby (2000) ArticleTitleThyroid hormone and central nervous system development J. Endocrinol. 165 1–8 Occurrence Handle10.1677/joe.0.1650001 Occurrence Handle10750030

    Article  PubMed  Google Scholar 

  • H. Cherif B. Reusens M. T. Ahn J. J. Hoet C. Remacle (1998) ArticleTitleEffects of taurine on the insulin secretion of rat fetal islets from dams fed a low protein diet J. Endocrinol. 159 341–348 Occurrence Handle10.1677/joe.0.1590341 Occurrence Handle9795376

    Article  PubMed  Google Scholar 

  • M. E. Cleasby P. A. T. Kelly B. R. Walker J. R. Seckl (2003) ArticleTitleProgramming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids Endocrinology 144 999–1007 Occurrence Handle10.1210/en.2002-220559 Occurrence Handle12586777

    Article  PubMed  Google Scholar 

  • M. A. Cowley J. L. Smart M. Rubinstein M. G. Cerdan S. Diano T. L. Horvath R. D. Cone M. J. Low (2001) ArticleTitleLeptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus Nature 411 480–484 Occurrence Handle10.1038/35078085 Occurrence Handle11373681

    Article  PubMed  Google Scholar 

  • C. O. Cravo C. V. Teixeira M. C. Passos S. C. Dutra E. G. Moura Particlede C. Ramos (2002) ArticleTitleLeptin treatment during the neonatal period is associated with higher food intake and.adult body weight in rats Horm. Metab. Res. 34 400–5 Occurrence Handle10.1055/s-2002-33473 Occurrence Handle12189589

    Article  PubMed  Google Scholar 

  • A. H. Coleoni N. Munaro A. R. Recupero O. Cherubini (1983) ArticleTitleNuclear trilothyronine receptors and metabolic response in perinatally protein-deprived rats Acta Endocrinol. 104 450–455 Occurrence Handle6318491

    PubMed  Google Scholar 

  • R. V. Considine M. K. Sinha M. L. Heiman A. Kriauciunas T. W. Stephens M. R. Nyce J. P. Ohannesian C. C. Marco L. J. McKee T. L. Bauer (1996) ArticleTitleSerum immunoreactive-leptin concentrations in normal-weight and obese humans N. Engl. J. Med. 334 292–295 Occurrence Handle10.1056/NEJM199602013340503 Occurrence Handle8532024

    Article  PubMed  Google Scholar 

  • W. S. Cutfield P. L. Hofman M. Vickers B. Breier W. F. Blum E. M. Robinson (2002) ArticleTitleIGFs and binding proteins in short children with intrauterine growth retardation J. Clin. Endocrinol. Metab. 87 235–239 Occurrence Handle10.1210/jc.87.1.235 Occurrence Handle11788652

    Article  PubMed  Google Scholar 

  • M. J. Dauncey P. White K. A. Burton M. Katsumata (2001) ArticleTitleNutrition-hormone receptor-gene interactions: implications for development and disease Proc. Nutr. Soc. 60 63–72 Occurrence Handle11310425

    PubMed  Google Scholar 

  • M. J. Dauncey K. A. Burton P. White A. P. Harrison R. S. Gilmour C. Duchamp D. Cattaneo (1994) ArticleTitleNutritional regulation of growth hormone receptor gene expression FASEB Journal 8 81–88 Occurrence Handle7507871

    PubMed  Google Scholar 

  • A. F. Debons I. Krimsky H. J. Likuski A. From R. J. Cloutier (1968) ArticleTitleGold thioglucose damage to the satiety center: inhibition in diabetes. sympathoadrenal response to acute hypoxia: impairment after experimental intrauterine Am. J. Physiol. 214 652–658 Occurrence Handle5638995

    PubMed  Google Scholar 

  • M. Desai C. N. Hales (1997) ArticleTitleRole of fetal and infant growth in programming metabolism in later life Biol. Rev. Cambridge Philos. Soc. 72 329–348 Occurrence Handle10.1017/S0006323196005026

    Article  Google Scholar 

  • S. C. P. Dutra M. C. F. Passos P. C. Lisboa A. P. Cabanelas R. Santos C. Pazos Moura E. G. Moura (2003) ArticleTitleLiver deiodinase activity is increased in adult rats whose mothers were submitted to malnutrition during lactation Horm. Metab. Res. 35 268–270 Occurrence Handle10.1055/s-2003-39485 Occurrence Handle12778372

    Article  PubMed  Google Scholar 

  • J. H. Dussault P. Coulombe P. Walker (1982) ArticleTitleEffects of neonatal hyperthyroidism on the development of the hypothalamic-pituitary-thyroid axis in the rat Endocrinology 110 1037–1042 Occurrence Handle6799277

    PubMed  Google Scholar 

  • J. C. Erickson G. Hollopeter R. D Palmiter (1996) ArticleTitleAttenuation of the obesity syndrome of ob/ob mice by the loss of neuropeptide Y Science 274 1704–1707 Occurrence Handle10.1126/science.274.5293.1704 Occurrence Handle8939859

    Article  PubMed  Google Scholar 

  • A. V. Ferguson W. L. Veale K. E. Cooper (1981) ArticleTitleEvidence of environmental influence on the development of thermoregulation in the rat Can. J. Physiol. Pharmacol. 59 91–95 Occurrence Handle7225948

    PubMed  Google Scholar 

  • A. C. Ferguson-Smith M. A. Surani (2001) ArticleTitleImprinting and the epigenetic asymmetry between parental genomes Science 293 1086–1089 Occurrence Handle10.1126/science.1064020 Occurrence Handle11498578

    Article  PubMed  Google Scholar 

  • D. A. Fisher J. H. Dussault J. Sack I. J. Chopra (1977) ArticleTitleOntogenesis of hypothalamic-pituitary-thyroid function and metabolism in man, sheep, and rat Recent Progr. Horm. Res. 33 59–116

    Google Scholar 

  • A. L Fowden (1995) ArticleTitleEndocrine regulation of fetal growth Reprod. Fertil. Dev. 7 351–363 Occurrence Handle10.1071/RD9950351 Occurrence Handle8606944

    Article  PubMed  Google Scholar 

  • J. M. Friedman J. L. Halaas (1998) ArticleTitleLeptin and the regulation of body weight in mammals Nature 395 763–770 Occurrence Handle10.1038/27376 Occurrence Handle9796811

    Article  PubMed  Google Scholar 

  • D. J Friedman F. Zeman (1979) ArticleTitleThyroid, pituitary, and hypothalamic hormone levelsin neonatal rat pups following maternal protein deficiency Proceedings of the Society for Experimental Biology and Medicine 16 275–279

    Google Scholar 

  • K. M. Godfrey D. J. P. Barker (2000) ArticleTitleFetal nutrition and adult disease Am. J. Clin. Nutr. 71 1344–1352

    Google Scholar 

  • C. N. Hales D. J. Barker (1992) ArticleTitleType 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis Diabetologia 35 595–601 Occurrence Handle10.1007/BF00400248 Occurrence Handle1644236

    Article  PubMed  Google Scholar 

  • C. N. Hales D. J. Barker P. M. Clark L. J. Cox C. Fall C. Osmond P.D. Winter (1991) ArticleTitleFetal and infant growth and impaired glucose tolerance at age 64 years Br. Med. J. 303 1019–1022

    Google Scholar 

  • A. R. Harris S.L. Fang F. Azizi L. Lpworth AG. Vagenakis L. E. Baverman (1978) ArticleTitleEffect of starvation on Hypothalamic-pituitary-thyroid function in the rat Metabolism 27 1074–1083 Occurrence Handle10.1016/0026-0495(78)90153-1 Occurrence Handle98684

    Article  PubMed  Google Scholar 

  • P. L. Hofman W. S. Cutfield E. M. Robinson R. N. Bergman R. K. Menon M. A. Sperling P. D. Gluckman (1997) ArticleTitleInsulin resistance in short children with intrauterine growth retardation J. Clin. Endocrinol Metab. 82 402–406 Occurrence Handle10.1210/jc.82.2.402 Occurrence Handle9024226

    Article  PubMed  Google Scholar 

  • K. Holemans J. Verhaeghe J. Dequeker F. A. Assche ParticleVan (1996) ArticleTitleInsulin sensitivity in adult female rats subjected to malnutrition during the perinatal period J. Soc. Gynecol. Invest. 3 71–77 Occurrence Handle10.1016/1071-5576(95)00046-1

    Article  Google Scholar 

  • M. J. Holness (1996) ArticleTitleThe effect of sub-optimal protein nutrition on insulin hypersecretion evoked by high-energy/high fat feeding in rats FEBS Lett. 396 53–56 Occurrence Handle10.1016/0014-5793(96)01067-8 Occurrence Handle8906865

    Article  PubMed  Google Scholar 

  • R. I. G. Holt (2002) ArticleTitleFetal programming of the growth hormone-insulin-like growth factor axis Trends Endocrinol. Metab. 13 392–397 Occurrence Handle10.1016/S1043-2760(02)00697-5 Occurrence Handle12367821

    Article  PubMed  Google Scholar 

  • R. I. Holt H. E. Syddall D. J. Phillips C. N. Martyn R. D. Gluckman B. H. Breier P. J. Wood C. H. Fall (2004) ArticleTitleSerum insulin-like growth factor-I concentrations in late middle age: no association with birthweight in three UK cohorts Acta Physiol. Scand. 180 359–66 Occurrence Handle10.1111/j.1365-201X.2004.01262.x Occurrence Handle15030377

    Article  PubMed  Google Scholar 

  • K. L. Houseknecht M. K. McGuire C. P. Portocarrero M. A. McGuire K. Beerman (1997) ArticleTitleLeptin is present in human milk and is related to maternal plasma leptin concentration and adiposity Biochem. Biophys. Res. Commun. 240 742–747 Occurrence Handle10.1006/bbrc.1997.7736 Occurrence Handle9398637

    Article  PubMed  Google Scholar 

  • B. V. Howard (1999) ArticleTitleInsulin resistance and lipid metabolism Am. J. Cardiol. 84 28J–32J Occurrence Handle10.1016/S0002-9149(99)00355-0 Occurrence Handle10418856

    Article  PubMed  Google Scholar 

  • J. J. Hwa A. B. Fawzi M. P. Graziano L. Ghibaudi P. Williams M. Heek Particlevan H. Davis M. Rudinski E. Sybertz C. D. Strader (1997) ArticleTitleLeptin increases energy expenditure and selectively promotes fat metabolism in ob/ob mice Am. J. Physiol. Regulatory Integrative Comp. Physiol. 272 1204–1209

    Google Scholar 

  • D. Huszar C. A. Lynch V. Fairchild-Huntress J. H. Dunmore Q. Fang L. R. Berkemeier W. Gu R. A. Kesterson B. A. Boston R. D. Cone F. J. Smith L. A. Campfield P. Burn F. Lee (1997) ArticleTitleTargeted disruption of the melanocortin-4 receptor results in obesity in mice Cell 88 131–141 Occurrence Handle10.1016/S0092-8674(00)81865-6 Occurrence Handle9019399

    Article  PubMed  Google Scholar 

  • L. Jin S. Zhang B. G. Burguera M. E. Couce R. Y. Osamura E. Kulig R. Lloyd (2000) ArticleTitleLeptin and leptin receptor expression in rat and mouse pituitary cells Endocrinology 141 333–339 Occurrence Handle10.1210/en.141.1.333 Occurrence Handle10614655

    Article  PubMed  Google Scholar 

  • T. Jolin L. Lamas (1984) ArticleTitleThyroid function in fasting rats Diabetes 33 383–388 Occurrence Handle6231204

    PubMed  Google Scholar 

  • M. Katsumata D. Cattaneo P. White K. A. Burton M. J. Dauncey (2000) ArticleTitleGrowth hormone receptor gene expression in porcine skeletal and cardiac muscles is selectively regulated by postnatal undernutrition J. Nutr. 130 2482–2488 Occurrence Handle11015477

    PubMed  Google Scholar 

  • S. C. Langley-Evans D. S. Gardner A. A. Jackson (1996) ArticleTitleAssociation of disproportionate growth of fetal rats in late gestation with raised systolic blood pressure in later life J. Reprod. Fertil. 106 307–312 Occurrence Handle8699415

    PubMed  Google Scholar 

  • G. Legradi C. H. Emerson R. S. Ahima J. S. Flier R. M. Lechan (1997) ArticleTitleLeptin prevents fasting-induced suppresion of prothyrotropin-releasing hormone messenger ribonucleic acid in neurons of the hypothalamic paraventricular nucleus Endocrinology 138 2569–2576 Occurrence Handle10.1210/en.138.6.2569 Occurrence Handle9165050

    Article  PubMed  Google Scholar 

  • J. Leger C. Levy-Marchal J. Bloch A. Pinet D. Chevenne D. Porquet D. Collin P. Czernichow (1997) ArticleTitleReduced final height and indications for insulin resistance in 20-year-olds born small for gestational age: regional cohort study Br. Med. J. 315 341–347

    Google Scholar 

  • N. S. Levitt R. S. Lindsay M. C. Holmes J. R. Seckl (1996) ArticleTitleDexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat Neuroendocrinology 64 412–418 Occurrence Handle8990073

    PubMed  Google Scholar 

  • J. Lesage L. Dufourny C. Laborie F. Bernet B. Blondeau I. Avril B. Breant J. P. Dupouy (2002) ArticleTitlePerinatal malnutrition programs sympathoadrenal and hypothalamic-pituitary-adrenal axis responsiveness to restraint stress in adult male rats J. Neuroendocrinol 14 135–143 Occurrence Handle10.1046/j.0007-1331.2001.00753.x Occurrence Handle11849373

    Article  PubMed  Google Scholar 

  • L. Ling E. B. Olson SuffixJr. E. H. Vidruk G. S. Mitchell (1996) ArticleTitleAttenuation of the hypoxic ventilatory response in adult rats following one month of perinatal hyperoxia J. Physiol. 495 561–571 Occurrence Handle8887766

    PubMed  Google Scholar 

  • R. Lingas S. G. Matthews (2001) ArticleTitleA short period of maternal nutrient restriction in late gestation modifies pituitary-adrenal function in adult guinea pig offspring Neuroendocrinology 73 302–311 Occurrence Handle10.1159/000054647 Occurrence Handle11399903

    Article  PubMed  Google Scholar 

  • H. O. Lithell P. M. McKeigue L. Berglund R. Mohsen U. B. Lithell D. A. Leon (1996) ArticleTitleRelation of size at birth to non insulin dependent diabetes and insulin concentrations in men aged 50–60 years Br. Med. J. 312 406–10

    Google Scholar 

  • P. C. Lisboa M. C. F. Passos S. C. P. Dutra R. S. Santos I. T. Bonomo A. P. Cabanelas C. C. Pazos-Moura E. G. Moura (2003) ArticleTitleIncreased 5′ iodothyronine deiodinase activity is a maternal adaptative mechanism in response to protein restriction during lactation J. Endocrinol. 177 261–267 Occurrence Handle10.1677/joe.0.1770261 Occurrence Handle12740014

    Article  PubMed  Google Scholar 

  • L. Liu A. Li S. G. Matthews (2001) ArticleTitleMaternal glucocorticoid treatment programs HPA regulation in adult offspring: sex-specific effects Am. J. Physiol. 280 E729–E739

    Google Scholar 

  • A. Lucas (1994) ArticleTitleRole of nutritional programming in determining adult morbidity Arch. Dis. Child 71 288–290 Occurrence Handle7979518

    PubMed  Google Scholar 

  • C. S. Mantzoros A. Varvarigou V. G. Kaklamani N. G. Beratis J. S. Flier (1997) ArticleTitleEffect of birthweight and maternal smoking on cord blood leptin concentrations of full-term and preterm newborns J. Clin. Endocrinol. Metab. 82 2856–2861 Occurrence Handle10.1210/jc.82.9.2856 Occurrence Handle9284710

    Article  PubMed  Google Scholar 

  • R. L. Martin E. Perez Y. J. He R. Dawson W. J. Millard (2000) ArticleTitleLeptin resistance is associated with hypothalamic leptin receptor mRNA and protein downregulation Metabolism 49 1479–1484 Occurrence Handle10.1053/meta.2000.17695 Occurrence Handle11092515

    Article  PubMed  Google Scholar 

  • S. G. Matthews (2000) ArticleTitleAntenatal glucocorticoids and programming of the developing CNS Pediatr. Res. 47 291–300 Occurrence Handle10709726

    PubMed  Google Scholar 

  • M. J. Meaney J. Diorio D. Francis S. Weaver J. Yau K. Chapman J. R. Seckl (2000) ArticleTitlePostnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin J. Neurosci. 20 3926–3935 Occurrence Handle10804232

    PubMed  Google Scholar 

  • M. J. Meaney (2001) ArticleTitleMaternal care, gene expression, and the transmission of individual differences in stress reactivity across generations Annu. Rev. Neurosci. 24 1161–1192 Occurrence Handle10.1146/annurev.neuro.24.1.1161 Occurrence Handle11520931

    Article  PubMed  Google Scholar 

  • B. Morash A. Li P. R. Murphy M. Wilkinson U. Ehud (1999) ArticleTitleLeptin gene expression in the brain and pituitary gland Endocrinology 1140 5995–5998 Occurrence Handle10.1210/en.140.12.5995

    Article  Google Scholar 

  • A. S. Moura J. S. Caldeira Filho P. C. Mathias C. C. N. Franco Sa Particlede (1997) ArticleTitleInsulin secretion impairment and insulin sensitivity improvement in adult rats undernourished during early lactation Res. Comm. Mol. Path Pharmacol. 96 180–192

    Google Scholar 

  • A. S. Moura C. C. Franco Sa Particlede H. G. Cruz C. L. Costa (2002) ArticleTitleMalnutrition during lactation as a metabolic imprinting factor inducing the feeding pattern of offspring rats when adults. The role of insulin and leptin Braz. J. Med. Biol. Res. 35 617–622 Occurrence Handle12011949

    PubMed  Google Scholar 

  • E. G. Moura C. F. Ramos C. C. A. Nascimento D. Rosenthal M. M. D. Breitenbach (1987) ArticleTitlefunction in fasting rats: variations in 1311 uptake and transient decrease in peroxidase activity Brazi. J. Med. Biol. Res. 20 407–410

    Google Scholar 

  • K. Muneoka M. Mikuni T. Ogawa K. Kitera K. Kamei M. Takigawa K. Takahashi (1997) ArticleTitlePrenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring Am. J. Physiol. 273 1669–1675

    Google Scholar 

  • M. J. Nyirenda R. S. Lindsay C. J. Kenyon A. Burchell J. R. Seckl (1998) ArticleTitleGlucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring J. Clin. Invest. 101 2174–2181 Occurrence Handle9593773

    PubMed  Google Scholar 

  • L. V. Oberkotter K. M. Rasmussen (1992) ArticleTitleChanges in plasma thyroid hormone concentration in chronically food-restricted female rats and their offspring during suckling J. Nutr. 122 435–441 Occurrence Handle1542002

    PubMed  Google Scholar 

  • J. H. Oppenheimer H. L. Schwartz (1997) ArticleTitleMolecular basis of thyroid hormone-dependent brain development Endocr. Rev. 18 462–475 Occurrence Handle10.1210/er.18.4.462 Occurrence Handle9267760

    Article  PubMed  Google Scholar 

  • T. M. Ortiga-Carvalho K. J. Oliveira B. A. Soares C. C. Pazos-Moura (2002) ArticleTitleLeptin role in the regulation of thyrotropin secretion in fed state – in vivo and in vitro studies J. Endocr. 174 121–125 Occurrence Handle10.1677/joe.0.1740121 Occurrence Handle12098670

    Article  PubMed  Google Scholar 

  • C. Osmond D. J. Barker P D. Winter C. H. Fall S. J. Simmonds (1993) ArticleTitleEarly growth and death from cardiovascular disease in women Br. Med. J. 307 1519–1524

    Google Scholar 

  • S. E. Ozanne M. W. Dorling C. L. Wang B. T. Nave (2001) ArticleTitleImpaired P13-kinase activation inadipocytes from early growth restricted male rats Am. J. Physiol. 280 E534–E539

    Google Scholar 

  • S. E. Ozanne N. Hales (2002) ArticleTitleEarly programming of glucose-insulinmetabolism Trend. Endocrinol. Metab. 13 368–373 Occurrence Handle10.1016/S1043-2760(02)00666-5

    Article  Google Scholar 

  • M. C. F. Passos C. F. Ramos E. G. Moura (2000) ArticleTitleShort and long term effects of malnutrition in rats during lactation on the body weight of offspring Nutr. Res. 20 1603–1612 Occurrence Handle10.1016/S0271-5317(00)00246-3

    Article  Google Scholar 

  • M. C. F. Passos C. F. Ramos T. Mouco E. G. Moura (2001a) ArticleTitleIncrease of T3 secreted through the milk in protein restricted lactating rats Nutr. Res. 21 917–924 Occurrence Handle10.1016/S0271-5317(01)00294-9

    Article  Google Scholar 

  • M. C. F. Passos C. F. Ramos S. C. P. Dutra T. Mouco E. G. Moura (2002) ArticleTitleLong term effects of malnutrition during lactation on the thyroid function of offspring Norm. Metab. Res. 34 40–43 Occurrence Handle10.1055/s-2002-19966

    Article  Google Scholar 

  • M. C. F. Passos L. L. Vicente P. C. Lisboa E. G. Moura (2004) ArticleTitleAbsence of anorectic effect to acute peripheral leptin treatment in adult animals whose mothers were malnourished during lactation Horm. Metab. Res. 36 625–629 Occurrence Handle10.1055/s-2004-825927 Occurrence Handle15486814

    Article  PubMed  Google Scholar 

  • D. I. Phillips D. J. Barker C. H. Fall J. R. Seckl C. B. Whorwood P. J. Wood B. R. Walker (1998) ArticleTitleElevated plasma cortisol concentrations: a link between low birthweight and the insulin resistance syndrome J. Clin. Endocrinol. Metab. 83 757–760 Occurrence Handle10.1210/jc.83.3.757 Occurrence Handle9506721

    Article  PubMed  Google Scholar 

  • D. I. Phillips D. J. Barker C. N. Hales S. Hirst C. Osmond (1994) ArticleTitleThinness at birth and insulin resistance in adult life Diabetologia 37 150–154 Occurrence Handle10.1007/s001250050086 Occurrence Handle8163048

    Article  PubMed  Google Scholar 

  • S. Pinto A. G. Roseberry H. Liu S. Diano M. Shanabrough X. Cai J. M. Friedman T. L. Horvath (2004) ArticleTitleRapid rewiring of arcuate nucleus feeding circuits by leptin Science 304 110–115 Occurrence Handle10.1126/science.1089459 Occurrence Handle15064421

    Article  PubMed  Google Scholar 

  • A. Plagemann I. Heidrich F. Gotz W. Rohde G. Dorner (1992) ArticleTitleObesity and enhanced diabetes and cardiovascular risk in adult rats due to early postnatal overfeeding Exp. Din. Endocrinol. 99 154–158

    Google Scholar 

  • A. Plagemann T. Harder A. Rake U. Janert K. Melchior W. Rohde G. Dorner (1999) ArticleTitleMorphological alterations of hypothalamic nuclei due to intrahypothalamic hyperinsulinism in newborn rats Int. J. Dev. Neurosci. 17 37–44 Occurrence Handle10.1016/S0736-5748(98)00064-1 Occurrence Handle10219959

    Article  PubMed  Google Scholar 

  • P. Poulsen A. A. Vaag K. O. Kyvik D. Moller Jensen H. Beck-Nielsen (1997) ArticleTitleLow birthweight is associated with NIDDM in discordant monozygotic and izygotic twin pairs Diabetologia 40 439–446 Occurrence Handle10.1007/s001250050698 Occurrence Handle9112021

    Article  PubMed  Google Scholar 

  • J. B. Pracyk F. J. Seidler E. C. McCook T. A. Slotkin (1992) ArticleTitlePituitary-thyroid axis reactivity to hyper- and hypothyroidism in the perinatal period: ontogeny of regulation of regulation and long-term programming of responses J. Dev. Physiol. 18 105–109 Occurrence Handle1301414

    PubMed  Google Scholar 

  • J. Rahier J. Wallon J. C. Henquin (1981) ArticleTitleCell populations of the endocrine pâncreas of human nenonates and infants Diabetologia 20 540–546 Occurrence Handle10.1007/BF00252762 Occurrence Handle6116638

    Article  PubMed  Google Scholar 

  • C. F. Ramos C.V. Teixeira M. C. F. Passos C. C. Pazos-Moura P. C. Lisboa F. H. Curty E. G. Moura (2000) ArticleTitleLow-Protein Diet changes Thyroid Function in Lactating Rats Proc. Soc. Exp. Biol. Med. .224 256–263 Occurrence Handle10.1046/j.1525-1373.2000.22429.x Occurrence Handle10964260

    Article  PubMed  Google Scholar 

  • C. F. Ramos A. P. S. Lima C. V. Teixeira P. D. Brito E. G. Moura (1997) ArticleTitleThyroid function in post-weaning rats, which dams were fed a low protein diet during suckling Braz. J. Med. Biol. Res. 30 133–137 Occurrence Handle10.1590/S0100-879X1997000100020 Occurrence Handle9222415

    Article  PubMed  Google Scholar 

  • G. K. Rastogi R. C. Sawhney N. C. Panda B. B. Tripathy (1974) ArticleTitleThyroid hormone levels in adult protein-calorie malnutrition (PCM) Horm. Metab. Res. 6 528–529 Occurrence Handle4217761

    PubMed  Google Scholar 

  • G. P. Ravelli Z. Stein M. Susser (1976) ArticleTitleObesity in young men after famine exposure in utero and early infancy N. Engl. J. Med. 295 349–353 Occurrence Handle934222

    PubMed  Google Scholar 

  • G. M. Reaven (1993) ArticleTitleRole of insulin resistance in human disease (syndrome X): an expanded definition Annu. Rev. Med. 44 121–131 Occurrence Handle10.1146/annurev.me.44.020193.001005 Occurrence Handle8476236

    Article  PubMed  Google Scholar 

  • M. A. Rostom Mello ParticleDe R. M. Oliveira Filho L. Cury L. B. S. Valle (1989) ArticleTitleCirculating thyroid hormone levels in young pregnant rats and their fetuses: Effect of malnutrition Ann. Nutr. Metab. 33 181–187 Occurrence Handle2802530

    PubMed  Google Scholar 

  • V. Rousseau D. J. Becker L. N. Ongemba J. Rahier J. C. Henquin S. M. Brichard (1997) ArticleTitleDevelopmental and nutritional changes of ob and PPAR gamma 2 gene expression in rat white adipose tissue Biochem. J. 321 451–456 Occurrence Handle9020880

    PubMed  Google Scholar 

  • R. Senaris T. Garcia-Caballero X. Casabiell R. Callero R. Castro R. V. Considine C. Dieguez F. F. Casanuera (1997) ArticleTitleSynthesis of leptin in human placenta Endocrinology 138 4501–4504 Occurrence Handle10.1210/en.138.10.4501 Occurrence Handle9322972

    Article  PubMed  Google Scholar 

  • L. M. Seoane E. Carro S. Tovar F. F. Casanueva C. Dieguez (2000) ArticleTitleRegulation in vivo TSH secretion by leptin Regul. Pept. 92 25–29 Occurrence Handle10.1016/S0167-0115(00)00145-2 Occurrence Handle11024561

    Article  PubMed  Google Scholar 

  • Shrader, R. E., Ferlatte, M. I., Hastings-Robertes M. H., Schoenborne, B. M., Hoernicke, C. A., and Zeman, F. J. (1997) Thyroid function in prenatally protein-deprived rats. J. Nutr. 107:221–229

    Google Scholar 

  • M. Sone H. Nagata S. Takekoshi R. Y. Osamura (2001) ArticleTitleExpression and localization of leptin receptor in the normal rat pituitary gland Cell Tissue Res. 305 351–356 Occurrence Handle10.1007/s004410100407 Occurrence Handle11572088

    Article  PubMed  Google Scholar 

  • S. M. Smith-Kirwin D. M. O’Connor J. Johnston ParticleDe E. D. Lancey ParticleDe S. G. Hassink V. L. Funanage (1998) ArticleTitleLeptin expression in human mammary epithelial cells and breast milk J. Clin. Endocrinol. Metab. 83 1810–1813 Occurrence Handle10.1210/jc.83.5.1810 Occurrence Handle9589698

    Article  PubMed  Google Scholar 

  • S. A. Stanner K. Bulmer C. Andrés (1997) ArticleTitleDoes malnutrition in utero determine diabetes and coronary heart disease in adulthood? Results from the Leningrad siege study, a cross sectional study Br. Med. J. 315 1342–1349

    Google Scholar 

  • Stephens, T. W., Basinski, M. Bristow, P. K. et al. (1995). The role of neuropeptide Y in the anti obesity action of the obese gene product. Nature 337:530–532

    Google Scholar 

  • M. C. Sugden M. L. Langdown M. J. Munns M. J. Holness (2001) ArticleTitleMaternal glucocorticoid treatment modulates placental leptin and leptin receptor expression and materno-fetal leptin physiology during late pregnancy, and elicits hypertension associated with hyperleptinaemia in the early-growth-retarded adult offspring Eur. J. Endocrinol. 145 529–539 Occurrence Handle10.1530/eje.0.1450529 Occurrence Handle11581014

    Article  PubMed  Google Scholar 

  • S. J. Swoap F. Haddad P. Bodell K. M. Baldwin (1994) ArticleTitleEffect of chronic energy deprivation on cardiac thyroid hormone receptor and myosin isoform expression Am. J. Physiol. 266 E254–E260 Occurrence Handle8141284

    PubMed  Google Scholar 

  • J. Tonkiss M. Trzcinska J. R. Galler N. Ruiz-Opazo (1998) ArticleTitlePrenatal malnutrition-induced changes in blood pressure: dissociation of stress and nonstress responses using radiotelemetry Hypertension 32 108–114 Occurrence Handle9674646

    PubMed  Google Scholar 

  • C. V. Teixeira M. C. F. Passos C. F. Ramos S. C. P. Dutra E. G. Moura (2002) ArticleTitleLeptin serum concentration in rats whose mothers were submitted to malnutrition during lactation J. Nutr. Biochem. 13 493–498 Occurrence Handle10.1016/S0955-2863(02)00197-3 Occurrence Handle12165362

    Article  PubMed  Google Scholar 

  • G. Trottier K. G. Koski T. Brun D. J. Toufexis D. Richard C. D. Walker (1998) ArticleTitleIncreased fat intake during lactation modifies hypothalamic-pituitary-adrenal responsiveness in developing rat pups: A possible role for leptin Endocrinology 139 3704–3711 Occurrence Handle10.1210/en.139.9.3704 Occurrence Handle9724021

    Article  PubMed  Google Scholar 

  • C. E. Tsai S. P. Lin M. Ito N. Takagi S. Takada A. C. Ferguson-Smith (2002) ArticleTitleGenomic imprinting contributes to thyroid hormone metabolism in the mouse embryo Curr. Biol. 23 1221–6 Occurrence Handle10.1016/S0960-9822(02)00951-X

    Article  Google Scholar 

  • S. K. Varma J. D. Crawford (1979) ArticleTitleLong-term perspectives of thyroxine administration in neonatal rats Horm. Res. 10 327–35 Occurrence Handle112019

    PubMed  Google Scholar 

  • M. Heek ParticleVan D. S. Compton C. F. France R. P. Tedesco A. B. Fawzi M. P. Graziano E. J. Sybertz C. D. Strader H. R. Davis SuffixJr. (1997) ArticleTitleDiet-induced obese mice develop peripheral but not central resistance to leptin J. Clin. Invest. 99 385–390 Occurrence Handle9022070

    PubMed  Google Scholar 

  • L. L. Vicente E. G. Moura P. C. Lisboa A. M. A. Costa T. Amadeu C. A. Mandarim-Lacerda M. C .F. Passos (2004) ArticleTitleMalnutrition during lactation is associated with higher expression of leptin receptor in pituitary of the adult rats Nutrition 20 924–928 Occurrence Handle15474883

    PubMed  Google Scholar 

  • P. Walker F. Courtin (1985) ArticleTitleTransient neonatal hyperthyroidism results in hypothyroidism in the adult rat Endocrinology 116 2246–2250 Occurrence Handle3996311

    PubMed  Google Scholar 

  • Wang, J., Liu, R., Hawkins, M., Barzilai, N. and Rosseti, L. (1998). A Nutrient sensing pathway regulates gene expression in muscle and fat. Nature 393: 684–688

    Google Scholar 

  • L. A. Welberg J. R. Seckl (2001) ArticleTitlePrenatal stress, glucocorticoids and the programming of the brain J. Neuroendocrinol. 13 113–128 Occurrence Handle10.1046/j.1365-2826.2001.00601.x Occurrence Handle11168837

    Article  PubMed  Google Scholar 

  • L. A. Welberg J. R. Seckl M. C. Holmes (2001) ArticleTitlePrenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour Neuroscience 104 71–79 Occurrence Handle10.1016/S0306-4522(01)00065-3 Occurrence Handle11311532

    Article  PubMed  Google Scholar 

  • M. Weinstock (2001) ArticleTitleAlterations induced by gestational stress in brain morphology and behaviour of the offspring Prog. Neurobiol. 65 427–451 Occurrence Handle10.1016/S0301-0082(01)00018-1 Occurrence Handle11689280

    Article  PubMed  Google Scholar 

  • P. A. Weller M. J. Dauncey P. C. Bates J. M. Brameld P. J. Buttery R. S. Gilmour (1994) ArticleTitleRegulation of porcine insulin-like growth factor I and growth hormone receptor mRNA expression by energy status Am. J. Physiol. 266 E776–E785 Occurrence Handle7515572

    PubMed  Google Scholar 

  • S. M. Woodall B. H. Breier B. M. Johnston P. D. Gluckman (1996) ArticleTitleA model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: effects on the somatotrophic axis and postnatal growth J. Endocrinol. 150 231–242 Occurrence Handle10.1677/joe.0.1500231 Occurrence Handle8869590

    Article  PubMed  Google Scholar 

  • J. B. Young (2002) ArticleTitleEffects of litter size on sympathetic activity in young adult rats Am. J. Physiol. Regul. lntegr. Comp. Physiol. 282 R1113–R1121

    Google Scholar 

  • J. B. Young L. Landsberg (1980) ArticleTitleImpaired suppression of sympathetic activity during fasting in the gold thioglucose-treated mouse J. Clin. Invest. 65 1086–1094 Occurrence Handle6102570

    PubMed  Google Scholar 

  • Y. Zhang R. Proenca M. Maffei (1994) ArticleTitlePositional cloning of the mouse obese gene and its homologue Nature 372 425–432 Occurrence Handle10.1038/372425a0 Occurrence Handle7984236

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dept. Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brasil

    Egberto Gaspar de Moura

  2. Dept. Nutrição Aplicada, Instituto de Nutrição, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brasil

    Magna Cottini F Passos

Authors
  1. Egberto Gaspar de Moura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Magna Cottini F Passos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Egberto Gaspar de Moura.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Moura, E.G., Passos, M.C.F. Neonatal Programming of Body Weight Regulation and Energetic Metabolism. Biosci Rep 25, 251–269 (2005). https://doi.org/10.1007/s10540-005-2888-3

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10540-005-2888-3

Keywords

Search

Navigation