Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring

American Journal of Physiology - Endocrinology and Metabolism

Volumn 296, Issue 3, 2009, Pages

  Breton, Christophe ^a   Lukaszewski, Marie Amélie ^a   Risold, Pierre Yves ^b   Enache, Mihaela ^a   Guillemot, Johann ^a   Rivière, Guillaume ^a   Delahaye, Fabien ^a   Lesage, Jean ^a   Dutriez Casteloot, Isabelle ^a   Laborie, Christine ^a   Vieau, Didier ^a  

^a UNIV LILLE   (France)

^b Expression Génique et Pathologies du Système Nerveux Central   (France)

Author keywords

Appetite programming; Arcuate nucleus; Feeding rhythm; Hypothalamus; Maternal undernutrition

Indexed keywords

BETA ENDORPHIN; CORTICOSTERONE; CYCLOPHILIN B; INSULIN RECEPTOR; LEPTIN RECEPTOR; MESSENGER RNA; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN; PROTEIN C FOS; HORMONE; INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APPETITE; ARCUATE NUCLEUS; ARTICLE; BODY COMPOSITION; BODY WEIGHT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DIET RESTRICTION; ENERGY BALANCE; ENERGY METABOLISM; FEMALE; FOOD INTAKE; GENE EXPRESSION; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HORMONE BLOOD LEVEL; HYPERINSULINEMIA; HYPERLEPTINEMIA; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; INSULIN RELEASE; INSULIN RESPONSE; LIPID STORAGE; MALE; MALNUTRITION; MATERNAL NUTRITION; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGENY; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BLOOD; CYTOLOGY; EATING; FEEDING BEHAVIOR; FETAL MALNUTRITION; GENETICS; LITTER SIZE; METABOLISM; ONCOGENE; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; WISTAR RAT;

ANIMALS; APPETITE; ARCUATE NUCLEUS; BETA-ENDORPHIN; BODY COMPOSITION; BODY WEIGHT; EATING; ENERGY METABOLISM; FEEDING BEHAVIOR; FEMALE; FETAL NUTRITION DISORDERS; GENES, FOS; GLUCOSE TOLERANCE TEST; HORMONES; INSULIN; LITTER SIZE; MALE; NEURONS; NEUROPEPTIDE Y; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRO-OPIOMELANOCORTIN; RATS; RATS, WISTAR; RECEPTOR, INSULIN; RECEPTORS, LEPTIN;

EID: 64749111414     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90740.2008     Document Type: Article

References (57)

1. Ahima RS, Kelly J, Elmquist JK, Flier JS. Distinct physiologic and neuronal responses to decreased leptin and mild hyperleptinemia. Endocrinology 140: 4923-4931, 1999. (Pubitemid 30660191)
2. Arora S, Anubhuti. Role of neuropeptides in appetite regulation and obesity. Neuropeptides 40: 375-401, 2006.
3. Attig L, Solomon G, Ferezou J, Abdennebi-Najar L, Taouis M, Gertler A, Djiane J. Early postnatal leptin blockage leads to a long-term leptin resistance and susceptibility to diet-induced obesity in rats. Int J Obes 32: 1153-1160, 2008.
4. Barker DJ. The developmental origins of chronic adult disease. Acta Paediatr 93: 26-33, 2004.
5. Bouret SG, Draper SJ, Simerly RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304: 108-110, 2004.
6. Breton C, Pechoux C, Morel G, Zingg HH. Oxytocin receptor messenger ribonucleic acid: characterization, regulation, and cellular localization in the rat pituitary gland. Endocrinology 136: 2928-2936, 1995.
7. Chen K, Li F, Li J, Cai H, Strom S, Bisello A, Kelley DE, Friedman- Einat M, Skibinski GA, McCrory MA, Szalai AJ, Zhao AZ. Induction of leptin resistance through direct interaction of C-reactive protein with leptin. Nat Med 12: 425-432, 2006.
8. Chrousos GP. Stressors: stress and neuroendocrine integration of the adaptative response. Ann NY Acad Sci 851: 311-335, 1998.
9. Cottrell EC, Ozanne SE. Developmental programming of energy balance and the metabolic syndrome. Proc Nutr Soc 66: 198-206, 2007.
10. Cripps RL, Archer ZA, Mercer JG, Ozanne SE. Early life programming of energy balance. Biochem Soc Trans 35: 1203-1205, 2007.
11. Delahaye F, Breton C, Risold PY, Enache M, Dutriez-Casteloot I, Laborie C, Lesage J, Vieau D. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology 149: 470-475, 2008.
12. de Moura EG, Passos MC. Neonatal programming of body weight regulation and energetic metabolism. Biosci Rep 25: 251-269, 2005.
13. Desai M, Gayle D, Han G, Ross MG. Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reprod Sci 14: 329-337, 2007.
14. Dutriez-Casteloot I, Breton C, Coupe B, Hawchar O, Enache M, Dickes-Coopman A, de Keyzer Y, Deloof S, Lesage J, Vieau D. Tissue-specific programming expression of glucocorticoid receptors and 11β-HSDs by maternal perinatal undernutrition in the HPA axis of adult male rats. Horm Metab Res 40: 1-5, 2008.
15. Elias CF, Aschkenasi C, Lee C, Kelly J, Ahima RS, Bjørbaek C, Flier JS, Saper CB, Elmquist JK. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron 23: 775-786, 1999. (Pubitemid 29411566)
16. Engelbregt MJT, van Weissenbruch MM, Lips P, van Lingen A, Roos JC, Delemarre-van de Waal HA. Body composition and bone measurements in intra-uterine growth-retarded and early postnatally undernourished male and female rats at the age of 6 months: comparison with puberty. Bone 34: 180-186, 2004. (Pubitemid 38142447)
17. Fernandez-Twinn DS, Ozanne SE. Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome. Physiol Behav 88: 234-243, 2006.
18. 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 Biol Sci 272: 671-677, 2005. (Pubitemid 41411124)
19. Heiman ML, Ahima RS, Craft LS, Schoner B, Stephens TW, Flier JS. Leptin inhibition of the hypothalamic-pituitary-adrenal axis in response to stress. Endocrinology 138: 3859-3863, 1997. (Pubitemid 27351940)
20. Hoet JJ, Hanson MA. Intrauterine nutrition: its importance during critical periods for cardiovascular and endocrine development. J Physiol 514: 617-627, 1999.
21. Houdijk ECAM, Engelbregt MJT, Popp-Snijders C, Delemarre-van de Waal HA. Endocrine regulation and extended follow-up of longitudinal growth in intrauterine growth-retarded rats. J Endocrinol 166: 599-608, 2000.
22. Ikenasio-Thorpe BA, Breier BH, Vickers MH, Fraser MH. Prenatal influences on susceptibility to diet-induced obesity are mediated by altered neuroendocrine gene expression. J Endocrinol 193: 31-37, 2007.
23. Jaferi A, Bhatnagar S. Corticosterone can act at the posterior paraventricular thalamus to inhibit hypothalamic-pituitary-adrenal activity in animals that habituate to repeated stress. Endocrinology 147: 4917-4930, 2006. (Pubitemid 44402199)
24. Jamali AK, Tramu G. Daily cycle of fos expression within hypothalamic POMC neurons of the male rat. Brain Res 771: 45-54, 1997. (Pubitemid 27465689)
25. Kind KL, Roberts CT, Sohlstrom AI, Katsman A, Clifton PM, Robinson JS, Owens JA. Chronic maternal feed restriction impairs growth but increases adiposity of the fetal guinea pig. Am J Physiol Regul Integr Comp Physiol 288: R119-R126, 2005. (Pubitemid 40023921)
26. Krechowec SO, Vickers MH, Gertler A, Breier BH. Prenatal influence on leptin sensitivity and susceptibility to diet-induced obesity. J Endocrinol 189: 355-363, 2006. (Pubitemid 43757793)
27. Ladyman SR. Leptin resistance during pregnancy in the rat. J Neuroendocrinol 20: 269-277, 2008.
28. Lesage J, Sebaai N, Léonhardt M, Dutriez-Casteloot I, Breton C, Deloof S, Vieau D. Perinatal maternal undernutrition programs the offspring hypothalamo-pituitary-adrenal (HPA) axis. Stress 9: 183-198, 2006. (Pubitemid 46005630)
29. Levin BE. Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos Trans R Soc Lond B Biol Sci 361: 1107-1121, 2006.
30. Lopez M, Seoane LM, Tovar S, Garcia MC, Nogueiras R, Dieguez C, Senaris RM. A possible role of neuropeptide Y, agouti-related protein and leptin receptor isoforms in hypothalamic programming by perinatal feeding in the rat. Diabetologia 48: 140-148, 2005. (Pubitemid 40174666)
31. Maccari S, Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32: S10-S15, 2007. (Pubitemid 47211641)
32. MohanKumar SM, King A, Shin AC, Sirivelu MP, MohanKumar PS, Fink GD. Developmental programming of cardiovascular disorders: focus on hypertension. Rev Endocr Metab Disord 8: 115-125, 2007. (Pubitemid 47434647)
33. Myers MG, Cowley MA, Münzberg H. Mechanisms of leptin action and leptin resistance. Annu Rev Physiol 70: 537-556, 2008.
34. Ohta H, Xu S, Moriya T, Iigo M, Watanabe T, Nakahata N, Chisaka H, Hanita T, Matsuda T, Ohura T, Kimura Y, Yaegashi N, Tsuchiya S, Tei H, Okamura K. Maternal feeding controls fetal biological clock. PLoS ONE 3: e2601, 2008.
35. Plagemann A, Harder T, Melchior K, Rake A, Rohde W, Dörner G. Elevation of hypothalamic neuropeptide Y neurons in adult offspring of diabetic mother rats. Neuroreport 10: 3211-3216, 1999. (Pubitemid 29498423)
36. Plagemann A, Harder T, Rake A, Janert U, Melchior K, Rohde W, Dörner G. Morphological alterations of hypothalamic nuclei due to intrahypothalamic hyperinsulinism in newborn rats. Int J Dev Neurosci 17: 37-44, 1999. (Pubitemid 29148279)
37. Plagemann A, Harder T, Rake A, Waas T, Melchior K, Rohde W, Dörner G. Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr 130: 2582-2589, 2000.
38. Plagemann A, Harder T, Rake A, Waas T, Melchior K, Ziska T, Rohde W, Dörner G. Observations on the orexigenic hypothalamic neuropeptide Y system in neonatally overfed weanling rats. J Neuroendocrinol 11: 541-546, 1999. (Pubitemid 29312847)
39. Plagemann A, Waas T, Harder T, Rittel F, Ziska T, Rohde W. Hypothalamic neuropeptide Y levels in weaning offspring of low-protein malnourished mother rats. Neuropeptides 34: 1-6, 2000. (Pubitemid 30164274)
40. Rajakumar PA, He J, Simmons RA, Devaskar SU. Effects of uteroplacental insufficiency upon brain neuropeptide Y and corticotropin-releasing factor gene expression and concentrations. Pediatr Res 44: 168-174, 1998. (Pubitemid 28347891)
41. 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 70: 811-816, 1999. (Pubitemid 29512905)
42. Remmers F, Verhagen LA, Adan RA, Delemarre-van de Waal HA. Hypothalamic neuropeptide expression of juvenile and middle-aged rats after early postnatal food restriction. Endocrinology 149: 3617-3625, 2008.
43. Reusens B, Ozanne SE, Remacle C. Fetal determinants of type 2 diabetes. Curr Drug Target 8: 935-941, 2007.
44. Rivière G, Michaud A, Breton C, VanCamp G, Laborie C, Enache M, Lesage J, Deloof S, Corvol P, Vieau D. Angiotensin-converting enzyme 2 (ACE2) and ACE activities display tissue-specific sensitivity to undernutrition- programmed hypertension in the adult rat. Hypertension 46: 1169-1174, 2005. (Pubitemid 41533021)
45. Sainsbury A, Cooney GJ, Herzog H. Hypothalamic regulation of energy homeostasis. Best Pract Res Clin Endocrinol Metab 16: 623-637, 2002. (Pubitemid 36040541)
46. Sebaai N, Lesage J, Breton C, Vieau D, Deloof S. Perinatal food deprivation induces marked alterations of the hypothalamo-pituitary-adrenal axis in 8-mo-old male rats both under basal conditions and after a dehydration period. Neuroendocrinology 79: 163-173, 2004. (Pubitemid 38698119)
47. Seckl JR. Prenatal glucocorticoids and long-term programming. Eur J Endocrinol 151: U49-U62, 2004.
48. Singru PS, Sanchez E, Fekete C, Lechan RM. Importance of melanocortin signaling in refeeding-induced neuronal activation and satiety. Endocrinology 148: 638-646, 2007. (Pubitemid 46143167)
49. Smart JL, Tolle V, Oteron-Corchon V, Low MJ. Central dysregulation of the hypothalamic-pituitary-adrenal axis in neuron-specific proopiomelanocortin- deficient mice. Endocrinology 148: 647-659, 2007. (Pubitemid 46143168)
50. Taylor PD, Poston L. Developmental programming of obesity in mammals. Exp Physiol 92: 287-298, 2007. (Pubitemid 46376323)
51. Thompson NM, Norman AM, Donkin SS, Shankar RR, Vickers MH, Miles JL, Breier BH. Prenatal and postnatal pathways to obesity: different underlying mechanisms, different metabolic outcomes. Endocrinology 148: 2345-2354, 2007.
52. van Dijk G, de Vries K, Nyakas C, Buwalda B, Adage T, Kuipers F, Kas MJH, Adan RAH, Wilkinson CW, Thiele TE, Scheurink AJW. Reduced anorexigenic efficacy of leptin, but not of the melanocortin receptor agonist melanotan-II, predicts diet-induced obesity in rats. Endocrinology 146: 5247-5256, 2005. (Pubitemid 41655946)
53. 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 279: E83-E87, 2000.
54. Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, Gertler A, Breier BH, Harris M. Neonatal leptin treatment reverses developmental programming. Endocrinology 146: 4211-4216, 2005. (Pubitemid 41324016)
55. Vickers MH, Ikenasio-Thorpe BA, Breier BH. Adult growth hormone treatment reduces hypertension and obesity by an adverse prenatal environment. J Endocrinol 175: 615-623, 2002.
56. Vuguin PM. Animal model for small for gestational age and fetal programming of adult disease. Horm Res 68: 113-123, 2007.
57. Yu IC, Lin HY, Liu NC, Wang RS, Sparks JD, Yeh SY, Chang C. Hyperleptinemia without obesity in male mice lacking androgen receptor in adipose tissue. Endocrinology 149: 2361-2368, 2008.