Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Orozco Solís, Ricardo ^a   Matos, Rhowena J B ^a   Guzmán Quevedo, Omar ^a   de Souza, Sandra Lopes ^b   Bihouée, Audrey ^c   Houlgatte, Rémi ^c   de Castro, Raul Manhães ^d   Bolaños Jiménez, Francisco ^a  

^a Universite de Nantes   (France)

^b DEPARTAMENTO DE MICOLOGIA   (Brazil)

^c L INSTITUT DU THORAX   (France)

^d FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE; BINDING PROTEIN; CARBOHYDRATE RESPONSE ELEMENT BINDING PROTEIN; CELL NUCLEUS RECEPTOR; CHOLESTEROL; FATTY ACID; FATTY ACID SYNTHASE; GENE PRODUCT; GLUCOCORTICOID RECEPTOR; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; NEUROTRANSMITTER RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; RETINOIC ACID RECEPTOR RELATED ORPHAN RECEPTOR ALPHA; RETINOIC ACID RECEPTOR RELATED ORPHAN RECEPTOR BETA; RETINOID X RECEPTOR ALPHA; STEAROYL COENZYME A DESATURASE 1; THYROID HORMONE RECEPTOR BETA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME; TRIACYLGLYCEROL; TUBERIN; UNCLASSIFIED DRUG;

ABDOMINAL FAT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CIRCADIAN RHYTHM; CLASSIFICATION; CONTROLLED STUDY; DOWN REGULATION; ENERGY HOMEOSTASIS; FATTY ACID BLOOD LEVEL; FEMALE; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HOMEOSTASIS; HYPOTHALAMUS; LACTATION; MALE; MATERNAL NUTRITION; METABOLIC REGULATION; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PREGNANCY; PROGENY; PROTEIN RESTRICTION; RAT; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; ANIMAL; DIET; ENERGY METABOLISM; GENE EXPRESSION PROFILING; METABOLISM; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; DIET; ENERGY METABOLISM; FEMALE; GENE EXPRESSION PROFILING; HOMEOSTASIS; HYPOTHALAMUS; MALE; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 78149440714     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013537     Document Type: Article

References (57)

1. Keith SW, Redden DT, Katzmarzyk PT, Boggiano MM, Hanlon EC, et al. (2006) Putative contributors to the secular increase in obesity: exploring the roads less traveled. Int J Obes (Lond) 30: 1585-1594.
2. Ravelli GP, Stein ZA, Susser MW (1976) Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 295: 349-353.
3. Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60: 5-20.
4. Gluckman PD, Hanson MA (2004) The developmental origins of the metabolic syndrome. Trends in Endocrinology and Metabolism 15: 183-187.
5. Bieswal F, Ahn M-T, Reusens B, Holvoet P, Raes M, et al. (2006) The Importance of Catch-up Growth after Early Malnutrition for the Programming of Obesity in Male Rat[ast]. Obesity 14: 1330-1343.
6. Zambrano E, Bautista C, Deás M, Martínez-Samayoa P, González-Zamorano M, et al (2006) A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol 15: 221-230.
7. Krechowec SO, Vickers M, Gertler A, Breier BH (2006) Prenatal influences on leptin sensitivity and susceptibility to diet-induced obesity. J Endocrinol 189: 355-363.
8. Desai M, Babu J, Ross MG (2007) Programmed metabolic syndrome: prenatal undernutrition and postweaning overnutrition. Am J Physiol Regul Integr Comp Physiol 293: R2306-2314.
9. Erhuma A, Salter AM, Sculley DV, Langley-Evans SC, Bennett AJ (2007) Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol Endocrinol Metab 292: E1702-1714.
10. McMullen S, Langley-Evans SC (2005) Maternal low-protein diet in rat pregnancy programs blood pressure through sex-specific mechanisms. Am J Physiol Regul Integr Comp Physiol 288: R85-90.
11. Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD (2000) Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 279: E83-87.
12. Desai M, Gayle D, Han G, Ross MG (2007) Programmed Hyperphagia Due to Reduced Anorexigenic Mechanisms in Intrauterine Growth-Restricted Off-spring. Reproductive Sciences 14: 329-337.
13. Bellinger L, Langley-Evans S (2005) Fetal programming of appetite by exposure to a maternal low-protein diet in the rat. Clin Sci (Lond) 109: 413-420.
14. Lopes de Souza S, Orozco-Solis R, Grit I, Manhaes de Castro R, Bolanos-Jimenez F (2008) Perinatal protein restriction reduces the inhibitory action of serotonin on food intake. European Journal of Neuroscience 27:1400-1408.
15. Orozco-Sólis R, Lopes de Souza S, Barbosa Matos RJ, Grit I, Le Bloch J, et al. (2009) Perinatal undernutrition-induced obesity is independent of the developmental programming of feeding. Physiology & Behavior 96: 481-492.
16. Plagemann A, Rittel F, Waas T, Harder T, Rohde W (1999) Cholecystokinin-8S levels in discrete hypothalamic nuclei of weanling rats exposed to maternal protein malnutrition. Regulatory Peptides 85: 109-113.
17. Plagemann A, Waas T, Harder T, Rittel F, Ziska T, et al. (2000) Hypothalamic neuropeptide Y levels in weaning offspring of low-protein malnourished mother rats. Neuropeptides 34: 1-6.
18. Ikenasio-Thorpe BA, Breier BH, Vickers MH, Fraser M (2007) Prenatal influences on susceptibility to diet-induced obesity are mediated by altered neuroendocrine gene expression. J Endocrinol 193: 31-37.
19. Plagemann A, Harder T, Rake A, Melchior K, Rohde W, et al. (2000) Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr 130: 2582-2589.
20. Yura S, Itoh H, Sagawa N, Yamamoto H, Masuzaki H, et al. (2005) Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab 1: 371-378.
21. Sardinha FLC, Telles MM, Albuquerque KT, Oyama LM, Guimarães PAMP, et al. Gender difference in the effect of intrauterine malnutrition on the central anorexigenic action of insulin in adult rats. Nutrition 22: 1152-1161.
22. Barabasi A-L, Oltvai ZN (2004) Network biology: understanding the cell's functional organization. Nat Rev Genet 5: 101-113.
23. Sieberts SK, Schadt EE (2007) Moving toward a system genetics view of disease. Mamm Genome 18: 389-401.
24. Man PS, Lawrence CB (2008) Galanin-like peptide: a role in the homeostatic regulation of energy balance? Neuropharmacology 55: 1-7.
25. Nogueiras R, Diaz-Arteaga A, Lockie SH, Velasquez DA, Tschop J, et al. (2009) The endocannabinoid system: role in glucose and energy metabolism. Pharmacol Res 60: 93-98.
26. Guard DB, Swartz TD, Ritter RC, Burns GA, Covasa M (2009) Blockade of hindbrain NMDA receptors containing NR2 subunits increases sucrose intake. Am J Physiol Regul Integr Comp Physiol 296: R921-928.
27. Jensen CB, Martin-Gronert MS, Storgaard H, Madsbad S, Vaag A, et al. (2008) Altered PI3-Kinase/Akt Signalling in Skeletal Muscle of Young Men with Low Birth Weight. PLoS ONE 3: e3738.
28. Sampaio de Freitas M, Garcia De Souza EP, Vargas da Silva S, da Rocha Kaezer A, da Silva Vieira R, et al. (2003) Up-regulation of phosphatidylinositol 3-kinase and glucose transporter 4 in muscle of rats subjected to maternal undernutrition. Biochim Biophys Acta 1639: 8-16.
29. Plum L, Ma X, Hampel B, Balthasar N, Coppari R, et al. (2006) Enhanced PIP3 signaling in POMC neurons causes KATP channel activation and leads to diet-sensitive obesity. J Clin Invest 116: 1886-1901.
30. Nikoulina SE, Ciaraldi TP, Mudaliar S, Mohideen P, Carter L, et al. (2000) Potential role of glycogen synthase kinase-3 in skeletal muscle insulin resistance of type 2 diabetes. Diabetes 49: 263-271.
31. Eldar-Finkelman H, Schreyer SA, Shinohara MM, LeBoeuf RC, Krebs EG (1999) Increased glycogen synthase kinase-3 activity in diabetes- and obesity- prone C57BL/6J mice. Diabetes 48: 1662-1666.
32. Morton GJ, Gelling RW, Niswender KD, Morrison CD, Rhodes CJ, et al. (2005) Leptin regulates insulin sensitivity via phosphatidylinositol-3-OH kinase signaling in mediobasal hypothalamic neurons. Cell Metab 2:411-420.
33. Wang C, Bomberg E, Billington C, Levine A, Kotz CM (2007) Brain-derived neurotrophic factor in the hypothalamic paraventricular nucleus reduces energy intake. Am J Physiol Regul Integr Comp Physiol 293: R1003-1012.
34. Unger TJ, Calderon GA, Bradley LC, Sena-Esteves M, Rios M (2007) Selective deletion of Bdnf in the ventromedial and dorsomedial hypothalamus of adult mice results in hyperphagic behavior and obesity. J Neurosci 27:14265-4274.
35. Lage R, Dieguez C, Vidal-Puig A, Lopez M (2008) AMPK: a metabolic gauge regulating whole-body energy homeostasis. Trends Mol Med 14: 539-549.
36. Woods SC, Seeley RJ, Cota D (2008) Regulation of Food Intake Through Hypothalamic Signaling Networks Involving mTOR. Annual Review of Nutrition 28: 295-311.
37. Inoki K, Li Y, Zhu T, Wu J, Guan KL (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4: 648-657.
38. Huang J, Manning BD (2009) A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochem Soc Trans 37: 217-222.
39. Desvergne B, Michalik L, Wahli W (2006) Transcriptional Regulation of Metabolism. Physiol Rev 86: 465-514.
40. Bookout AL, Jeong Y, Downes M, Yu RT, Evans RM, et al. (2006) Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 126: 789-799.
41. Sato T, Matsumoto T, Yamada T, Watanabe T, Kawano H, et al. (2003) Late onset of obesity in male androgen receptor-deficient (AR KO) mice. Biochem Biophys Res Commun 300: 167-171.
42. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS (2000) Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc Natl Acad Sci USA 97: 12729-12734.
43. Musatov S, Chen W, Pfaff DW, Mobbs CV, Yang XJ, et al. (2007) Silencing of estrogen receptor alpha in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci USA 104: 2501-2506.
44. Schibler U, Sassone-Corsi P (2002) A Web of Circadian Pacemakers. Cell 111: 919-922.
45. Preitner N, Damiola F, Luis Lopez M, Zakany J, Duboule D, et al. (2002) The Orphan Nuclear Receptor REV-ERB[alpha] Controls Circadian Transcription within the Positive Limb of the Mammalian Circadian Oscillator. Cell 110: 251-260.
46. Akashi M, Takumi T (2005) The orphan nuclear receptor ROR[alpha] regulates circadian transcription of the mammalian core-clock Bmal1. Nat Struct Mol Biol 12: 441-448.
47. Liu C, Li S, Liu T, Borjigin J, Lin JD (2007) Transcriptional coactivator PGC-1[agr] integrates the mammalian clock and energy metabolism. Nature 447:477-481.
48. Orozco-Sólis R, Barbosa Matos RJ, Lopes de Souza S, Grit I, Kaeffer B, et al. (2010) Perinatal nutrient restriction induces long-lasting alterations in the circadian expression pattern of genes regulating food intake and energy metabolism. International Journal of Obesity (In press).
49. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, et al. (2002) Coordinated Transcription of Key Pathways in the Mouse by the Circadian Clock. Cell 109: 307-320.
50. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, et al. (2005) Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308: 1043-1045.
51. Levin BE, Dunn-Meynell AA, Routh VH (2001) Brain glucosensing and the K(ATP) channel. Nat Neurosci 4: 459-460.
52. Xu AW, Kaelin CB, Takeda K, Akira S, Schwartz MW, et al. (2005) PI3K integrates the action of insulin and leptin on hypothalamic neurons. J Clin Invest 115: 951-958.
53. Claret M, Smith MA, Batterham RL, Selman C, Choudhury AI, et al. (2007) AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons. The Journal of Clinical Investigation 117: 2325-2336.
54. Morrison CD, Morton GJ, Niswender KD, Gelling RW, Schwartz MW (2005) Leptin inhibits hypothalamic Npy and Agrp gene expression via a mechanism that requires phosphatidylinositol 3-OH-kinase signaling. Am J Physiol En-docrinol Metab 289: E1051-1057.
55. Oldham MC, Konopka G, Iwamoto K, Langfelder P, Kato T, et al. (2008) Functional organization of the transcriptome in human brain. Nat Neurosci 11: 1271-1282.
56. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the United States of America 95: 14863-14868.
57. Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-[Delta][Delta]CT Method. Methods 25: 402-408.