Maternal prenatal undernutrition programs adipose tissue gene expression in adult male rat offspring under high-fat diet

American Journal of Physiology - Endocrinology and Metabolism

Volumn 301, Issue 3, 2011, Pages

  Lukaszewski, Marie Amélie ^a   Mayeur, Sylvain ^a   Fajardy, Isabelle ^a   Delahaye, Fabien ^a   Dutriez Casteloot, Isabelle ^a   Montel, Valérie ^a   Dickes Coopman, Anne ^a   Laborie, Christine ^a   Lesage, Jean ^a   Vieau, Didier ^a   Breton, Christophe ^a  

^a UNIVERSITÉ DE LILLE   (France)

Author keywords

Maternal undernutrition

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; 11BETA HYDROXYSTEROID DEHYDROGENASE 2; CORTICOSTERONE; LEPTIN; STAT3 PROTEIN;

ADIPOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATCH UP GROWTH; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HYPERLEPTINEMIA; LIPID DIET; MALE; MALNUTRITION; MATERNAL NUTRITION; METABOLIC SYNDROME X; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PHENOTYPE; PRENATAL PERIOD; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; WHITE ADIPOSE TISSUE;

EID: 80052043828     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00011.2011     Document Type: Article

References (65)

1. Ahima RS, Singhal NS. Adipokines that link obesity and diabetes to the hypothalamus. Prog Brain Res 153: 155-174, 2006.
2. Barker DJ. The developmental origins of chronic adult disease. Acta Paediatr 93: 26-33, 2004.
3. Bieswal F, Hay SM, McKinnon C, Reusens B, Cuignet M, Rees WD, Remacle C. Prenatal protein restriction does not affect the proliferation and differentiation of rat preadipocytes. J Nutr 134: 1493-1499, 2004.
4. Bol VV, Delattre AI, Reusens B, Raes M, Remacle C. Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am J Physiol Regul Integr Comp Physiol 297: R291-R299, 2009.
5. Boullu-Ciocca S, Dutour A, Guillaume V, Achard V, Oliver Grino MC. Postnatal diet-induced obesity in rats upregulates systemic and adipose tissue glucocorticoid metabolism during development and in adulthood. Diabetes 54: 197-203, 2005.
6. Boullu-Ciocca S, Achard V, Tassistro V, Dutour A, Grino M. Postnatal programming of glucocorticoid metabolism in rats modulates high-fat diet-induced regulation of visceral adipose tissue glucocorticoid exposure and sensitivity and adiponectin and proinflammatory adipokines gene expression in adulthood. Diabetes 57: 669-677, 2008.
7. Bouret SG, Draper SJ, Simerly RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304: 108-110, 2004.
8. Breton C, Lukaszewski MA, Risold PY, Enache M, Guillemot J, Rivière G, Delahaye F, Lesage J, Dutriez-Casteloot I, Laborie C, Vieau D. Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. Am J Physiol Endocrinol Metab 296: E462-E472, 2009.
9. Chakraborty S, Joseph DV, Bankart MJ, Petersen SA, Wailoo MP. Fetal growth restriction: relation to growth and obesity at the age of 9 years. Arch Dis Child Fetal Neonatal 92: F479-F483, 2007.
10. Cleasby ME, Kelly PAT, Walker BR, Seckl JR. Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids. Endocrinology 144: 999-1007, 2003.
11. Cottrell EC, Ozanne SE. Developmental programming of energy balance and the metabolic syndrome. Proc Nutr Soc 66: 198-206, 2007.
12. Coupé B, Amarger V, Grit I, Benani A, Parnet P. Nutritional programming affects hypothalamic organization and early response to leptin. Neuroendocrinology 151: 702-713, 2010.
13. Coupé B, Grit I, Darmaun D, Parnet P. The timing of "catch-up growth" and appetite regulation in male born with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol 297: R813-R824, 2009.
14. Davies JS, Kotokorpi P, Eccles SR, Barnes SK, Tokarczuk PF, Allen SK, Withworth HS, Gushina IA, Evans BAJ, Mode A, Zigman JM, Wells T. Ghrelin induces abdominal obesity via GHS-R-dependent lipid retention. Mol Endocrinol 23: 914-924, 2009.
15. 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.
16. Delahaye F, Lukaszewski MA, Dutriez-Casteloot I, Montel V, Dickes-Coopman A, Laborie C, Lesage J, Breton C, Vieau D. Maternal perinatal undernutrition programs a "brown-like" phenotype of gonadal white fat in male rat at weaning. Am J Physiol Regul Integr Comp Physiol 299: R101-R110, 2010.
17. 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.
18. Desai M, Guang H, Ferelli M, Kallichanda N, Lane RH. Programmed upregulation of adipogenic transcription factors in intrauterine growthrestricted offspring. Reprod Sci 15: 785-796, 2008.
19. Drake AJ, Raubenheimer PJ, Kerrigan D, Mclnnes KJ, Seckl JR, Walker BR. Prenatal dexamethasone programs expression of genes in liver and adipose tissue and increased hepatic lipid accumulation but not obesity on a high-fat diet. Endocrinology 151: 1581-1587, 2010.
20. Duque-Guimarães DE, de Castro J, Martinez-Botas J, Sardinha FL, Ramos MP, Herrera E, do Carmo MG. Early and prolonged intake of partially hydrogenated fat alters the expression of genes in rat adipose tissue. Nutrition 25: 782-789, 2009.
21. Dutriez-Casteloot I, Breton C, Coupé 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 11_-HSDs by maternal perinatal undernutrition in the HPA axis of adult male rats. Horm Metab Res 40: 1-5, 2008.
22. 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.
23. Gnanalingham MG, Mostlyn A, Symonds ME, Stephenson T. Ontogeny and nutritional programming of adiposity in sheep: potential role of. glucocorticoid action and uncoupling protein-2. Am J Physiol Regul Integr Comp Physiol 289: R1407-R1415, 2005.
24. 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. Obesity 18: 1593-1600, 2010.
25. Grayson BE, Kievit P, Smith MS, Grove KL. Critical hypothalamic appetitive development and expression: species considerations. Front Neuroendocrinol 31: 16-31, 2010.
26. Guan H, Arany E, van Beek JP, Chamson-Reig A, Thyssen S, Hill DJ, Yang K. Adipose tissue gene expression profiling reveals distinct molecular pathways that define visceral adiposity in offspring of maternal protein-restricted rats. Am J Physiol Endocrinol Metab 288: E663-E673, 2005.
27. Hoggard N, Hunter L, Duncan JS, Rayner DV. Regulation of adipose tissue leptin secretion by _-melanocyte-stimulating hormone and agoutirelated protein: further evidence of an interaction between leptin and the melanocortin signalling system. J Mol Endocrinol 32: 145-153, 2004.
28. Huan JN, Li J, Han Y, Chen K, Wu N, Zhao AZ. Adipocyte-selective reduction of the leptin receptors induced by antisense RNA leads to increased adiposity, dyslipidemia, and insulin resistance. J Biol Chem 278: 45638-45650, 2003.
29. Ibanez L. Early Development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. J Clin Endocrinol Metab 91: 2153-2158, 2006.
30. Jaquet D, Deghmoun S, Chevenne D, Collin D, Czernichow P, Lévy-Marchal C. Dynamic change in adiposity from fetal to postnatal life is involved in the metabolic syndrome associated with reduced fetal growth. Diabetologia 48: 849-855, 2005.
31. Jiang L, Wang Q, Yu Y, Zhao f Huang P, Zeng R, Qi RZ, Li W, Liu Y. Leptin contributes to the adaptive responses of mice to high-fat diet intake through suppressing the lipogenic pathway. PLoS One 4: e6884, 2009.
32. Joss-Moore LA, Wang Y, Campbell MS, Moore B, Yu X, Callaway CW, McKnight RA, Desai M, Moyer-Mileur LJ, Lane RH. Uteroplacental insufficiency increases visceral adiposity and visceral adipose PPARgamma2 expression in male rat offspring prior to the onset of obesity. Early Hum Dev 3: 179-185, 2010.
33. Kershaw EE, Morton NM, Dhillon H, Ramage L, Seckl JR, Flier JS. Adipocyte-specific glucocorticoid inactivation protects against diet-induced obesity. Diabetes 54: 1023-1031, 2005.
34. Kim YJ, Park T. Genes are differentially expressed in the epididymal fat of rats rendered obese by a high-fat diet. Nutrition Res 28: 414-422, 2008.
35. 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.
36. Li J, Yu X, Pan W, Unger RH. Gene expression profile of rat adipose tissue at the onset of high-fat-diet obesity. Am J Physiol Endocrinol Metab 282: E1334-E1341, 2002.
37. Lumbers ER, Yu ZY, Gibson KJ. The selfish brain and the Barker hypothesis. Clin Exp Pharmacol Physiol 28: 942-947, 2001.
38. Macfarlane DP, Forbes S, Walker SF. Glucocorticoids and fatty acid metabolism in humans: fuelling fat redistribution in the metabolic syndrome. J Endocrinol 197: 189-204, 2008.
39. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, Seckl JR, Flier JS. A transgenic model of visceral obesity and the metabolic syndrome. Science 294: 2166-2170, 2001.
40. Milagro FI, Campion J, Martinez A. 11-_-Hydroxysteroid dehydrogenase type 2 expression in white adipose tissue is strongly correlated with adiposity. J Steroid Biochem Mol Biol 104: 81-84, 2007.
41. Morris TJ, Vickers M, Gluckman P, Gilmour S, Affara N. Transcriptional profiling of rats subjected to gestational undernourishment: implications for the developmental variations in metabolic traits. PLoS One 4: e7271, 2009.
42. Muhlhausler B, Smith SR. Early-life origin of metabolic dysfunction: role of the adipocyte. Trends Endocrinol Metab 2: 51-57, 2009.
43. Nieuwenuizen AG, Rutters F. The hypothalamic-pituitary-adrenal-axis in the regulation of energy balance. Physiol Behav 94: 169-177, 2008.
44. Nyirenda MJ, Carter R, Tang JI, de Vries A, Schlumbohm C, Hillier SG, Streit F, Oellerich M, Armstrong VW, Seckl JR. Prenatal programming of metabolic syndrome in the common marmoset is associated with increased expression of 11_-hydroxysteroid dehydrogenase type 1. Diabetes 58: 2873-2879, 2009.
45. Ortega FJ, Mayas D, Moreno-Navarrete JM, Catalán V, Gómez-Ambrosi J, Esteve E, Rodriguez-Hermosa JI, Ruiz B, Ricart W, Peral B, Fruhbeck G, Tinahones FJ, Fernández-Real JM. The gene expression of the main lipogenic enzymes is downregulated in visceral adipose tissue of obese subjects. Obesity 18: 13-20, 2010.
46. Ozanne SE, Dorling MW, Wang CL, Nave BT. Impaired PI 3-kinase activation in adipocytes from early growth-restricted male rats. Am J Physiol Endocrinol Metab 280: E534-E539, 2001.
47. Pico C, Sanchez J, Oliver P, Palou A. Leptin production by the stomach is up-regulated in obese (fa/fa) Zucker rats. Obes Res 10: 932-938, 2002.
48. 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.
49. Prior LJ, Velkoska E, Watts R, Cameron-Smith D, Morris MJ. Undernutrition during suckling in rats elevates plasma adiponectin and its receptor in skeletal muscle regardless of diet composition: a protective effect? Int J Obes 32: 1585-1594, 2008.
50. 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.
51. 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.
52. 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.
53. Sebaai N, Lesage J, Breton C, Vieau D, Deloof S. 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 79: 163-173, 2004.
54. Simmons R. Developmental origins of adult metabolic disease. Endocrinol Metab Clin North Am 35: 193-204, 2006.
55. Soukas A, Cohen P, Socci ND, Friedman JM. Leptin-specific patterns of gene expression in white adipose tissue. Genes Dev 14: 963-980, 2000.
56. Lee MJ, Fried SK, Mundt SS, Wang Y, Sullivan S, Stefanni A, Daugherty BL, Hermanowski-Vosatka A. Depot-specific regulation of the conversion of cortisone to cortisol in human adipose tissue. Obesity 16: 1178-1185, 2008.
57. 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.
58. Vuguin PM. Animal model for small for gestational age and fetal programming of adult disease. Horm Res 68: 113-123, 2007.
59. Wake DJ, Walker BR. 11_-Hydroxysteroid dehydrogenase type 1 in obesity and the metabolic syndrome. Mol Cell Endocrinol 215: 45-54, 2004.
60. Wang P, Mariman E, Renes J, Keijer J. The secretory function of adipocytes in the physiology of white adipose tissue. J Cell Physiol 216: 3-13, 2008.
61. Wang MY, Orci L, Ravazzola M, Unger RH. Fat storage in adipocyte requires inactivation of leptin's paracrine activity: implications for treatment of human obesity. Proc Natl Acad Sci USA 102: 18011-18016, 2005.
62. Yang K, Guan H, Arany E, Hill DJ, Xiang Cao. Neuropeptide Y is produced in visceral adipose tissue and promotes proliferation of adipocyte precursor cells via the Y1 receptor. FASEB J 22: 2452-2464, 2008.
63. Yang YS, Song HD, Li RY, Zhou LB, Zhu ZD, Hu RM, Han ZG, Chen JL. The gene expression profiling of human visceral adipose tissue and its secretory functions. Biochem Biophys Res Commun 300: 839-846, 2003.
64. Zennaro MC, Caprio M, Fève B. Mineralocorticoid receptors in the metabolic syndrome. Trends Endocrinol Metab 20: 444-451, 2009.
65. Zhang T, Guan H, Arany E, Hill DJ, Yang K. Maternal protein restriction permanently programs adipocyte growth and development in adult male rat offspring. J Cell Biochem 101: 381-388, 2007.