Excess of Methyl Donor in the Perinatal Period Reduces Postnatal Leptin Secretion in Rat and Interacts with the Effect of Protein Content in Diet

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Giudicelli, Fanny ^a,b   Brabant, Anne Laure ^a,b   Grit, Isabelle ^a,b   Parnet, Patricia ^a,b   Amarger, Valérie ^a,b  

^a Universite de Nantes   (France)

^b UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; LEPTIN; METHYL GROUP; TRACE ELEMENT;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENERGY BALANCE; FEMALE; FOOD INTAKE; GROWTH DISORDER; HORMONE RELEASE; INSULIN BLOOD LEVEL; LACTATION; MACRONUTRIENT; MALE; MARE; MATERNAL NUTRITION; METHYLATION; NONHUMAN; PERINATAL PERIOD; POSTNATAL GROWTH; PREGNANCY; PROGENY; PROMOTER REGION; PROTEIN CONTENT; PROTEIN RESTRICTION; RAT; SEX DIFFERENCE; WEIGHT GAIN;

ANIMALS; BASE SEQUENCE; BODY WEIGHT; DIET; DIETARY PROTEINS; DIETARY SUPPLEMENTS; DNA METHYLATION; EATING; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LACTATION; LEPTIN; LITTER SIZE; MALE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 84879716847     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068268     Document Type: Article

References (53)

1. Hales CN, Barker DJ, (2001) The thrifty phenotype hypothesis. Br Med Bull 60: 5-20. doi:10.1093/bmb/60.1.5. PubMed: 11809615.
2. Ozanne SE, Hales CN, (2002) Early programming of glucose-insulin metabolism. Trends Endocrinol Metab 13: 368-373. doi:10.1016/S1043-2760(02)00666-5. PubMed: 12367817.
3. Symonds ME, Sebert SP, Hyatt MA, Budge H, (2009) Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol 5: 604-610. doi:10.1038/nrendo.2009.195. PubMed: 19786987.
4. Eriksson JG, Forsén T, Tuomilehto J, Osmond C, Barker DJ, (2001) Early growth and coronary heart disease in later life: longitudinal study. BMJ 322: 949-953. doi:10.1136/bmj.322.7292.949. PubMed: 11312225.
5. Gluckman PD, Hanson MA, (2004) The developmental origins of the metabolic syndrome. Trends Endocrinol Metab 15: 183-187. doi:10.1016/j.tem.2004.03.002. PubMed: 15109618.
6. Barker DJ, (2004) The developmental origins of adult disease. J Am Coll Nutr 23: 588S-595S. PubMed: 15640511.
7. Orozco-Solís R, Matos RJ, Guzmán-Quevedo O, Lopes de Souza S, Bihouée A, et al. (2010) Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus. PLOS ONE 5: e13537. doi:10.1371/journal.pone.0013537. PubMed: 20975839.
8. Qasem RJ, Cherala G, D'Mello AP, (2010) Maternal protein restriction during pregnancy and lactation in rats imprints long-term reduction in hepatic lipid content selectively in the male offspring. Nutr Res 30: 410-417. doi:10.1016/j.nutres.2010.05.008. PubMed: 20650349.
9. Martin-Gronert MS, Tarry-Adkins JL, Cripps RL, Chen JH, Ozanne SE, (2008) Maternal protein restriction leads to early life alterations in the expression of key molecules involved in the aging process in rat offspring. Am J Physiol Regul Integr Comp Physiol 294: R494-R500. PubMed: 18094069.
10. Langley-Evans SC, Bellinger L, McMullen S, (2005) Animal models of programming: early life influences on appetite and feeding behaviour. Matern Child Nutr 1: 142-148. doi:10.1111/j.1740-8709.2005.00015.x. PubMed: 16881893.
11. Delahaye F, Breton C, Risold PY, Enache M, Dutriez-Casteloot I, et al. (2008) 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. PubMed: 18006626.
12. Warner MJ, Ozanne SE, (2010) Mechanisms involved in the developmental programming of adulthood disease. Biochem J 427: 333-347. doi:10.1042/BJ20091861. PubMed: 20388123.
13. Vaiman D, Gascoin-Lachambre G, Boubred F, Mondon F, Feuerstein JM, et al. (2011) The intensity of IUGR-induced transcriptome deregulations is inversely correlated with the onset of organ function in a rat model. PLOS ONE 6: e21222. doi:10.1371/journal.pone.0021222. PubMed: 21731679.
14. Coupé B, Delamaire E, Hoebler C, Grit I, Even P, et al. (2011) Hypothalamus integrity and appetite regulation in low birth weight rats reared artificially on a high-protein milk formula. J Nutr Biochem 22: 956-963. doi:10.1016/j.jnutbio.2010.08.007. PubMed: 21167701.
15. Bol VV, Delattre AI, Reusens B, Raes M, Remacle C, (2009) 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. doi:10.1152/ajpregu.90497.2008. PubMed: 19458276.
16. Coupé B, Amarger V, Grit I, Benani A, Parnet P, (2010) Nutritional programming affects hypothalamic organization and early response to leptin. Endocrinology 151: 702-713. doi:10.1210/en.2009-0893. PubMed: 20016030.
17. Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, et al. (2007) Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr 97: 435-439. doi:10.1017/S0007114507352392. PubMed: 17313703.
18. Jousse C, Parry L, Lambert-Langlais S, Maurin AC, Averous J, et al. (2011) Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: Implication for the understanding of metabolic syndrome. FASEB J 25: 3271-3278. doi:10.1096/fj.11-181792. PubMed: 21670064.
19. van Straten EM, Bloks VW, Huijkman NC, Baller JF, van Meer H, et al. (2010) The liver X-receptor gene promoter is hypermethylated in a mouse model of prenatal protein restriction. Am J Physiol Regul Integr Comp Physiol 298: R275-R282. doi:10.1152/ajpregu.00413.2009. PubMed: 19889862.
20. Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, et al. (2008) Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr 100: 278-282. PubMed: 18186951.
21. Gabory A, Attig L, Junien C, (2011) Developmental programming and epigenetics. Am J Clin Nutr 94: 1943S-1952S. doi:10.3945/ajcn.110.000927. PubMed: 22049164.
22. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC, (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135: 1382-1386. PubMed: 15930441.
23. Torrens C, Brawley L, Anthony FW, Dance CS, Dunn R, et al. (2006) Folate supplementation during pregnancy improves offspring cardiovascular dysfunction induced by protein restriction. Hypertension 47: 982-987. doi:10.1161/01.HYP.0000215580.43711.d1. PubMed: 16585422.
24. Jackson AA, Dunn RL, Marchand MC, Langley-Evans SC, (2002) Increased systolic blood pressure in rats induced by a maternal low-protein diet is reversed by dietary supplementation with glycine. Clin Sci (Lond) 103: 633-639. PubMed: 12444916.
25. Davison JM, Mellott TJ, Kovacheva VP, Blusztajn JK, (2009) Gestational choline supply regulates methylation of histone H3, expression of histone methyltransferases G9a (Kmt1c) and Suv39h1 (Kmt1a), and DNA methylation of their genes in rat fetal liver and brain. J Biol Chem 284: 1982-1989. PubMed: 19001366.
26. Jiang X, Yan J, West AA, Perry CA, Malysheva OV, et al. (2012) Maternal choline intake alters the epigenetic state of fetal cortisol-regulating genes in humans. FASEB J 26: 3563-3574. doi:10.1096/fj.12-207894. PubMed: 22549509.
27. Niculescu MD, Craciunescu CN, Zeisel SH, (2006) Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. FASEB J 20: 43-49. doi:10.1096/fj.05-4707com. PubMed: 16394266.
28. Greenberg JA, Bell SJ, Guan Y, Yu YH, (2011) Folic Acid supplementation and pregnancy: more than just neural tube defect prevention. Rev Obstet Gynecol 4: 52-59. PubMed: 22102928.
29. Bakker R, Timmermans S, Steegers EA, Hofman A, Jaddoe VW, (2011) Folic acid supplements modify the adverse effects of maternal smoking on fetal growth and neonatal complications. J Nutr 141: 2172-2179. doi:10.3945/jn.111.142976. PubMed: 22031658.
30. Furness D, Fenech M, Dekker G, Khong TY, Roberts C, et al. (2011). Folate Vitamin B12Vitamin B6 and homocysteine: Impact on pregnancy outcome. Child Matern, eds. Nutr.
31. Shah PS, Ohlsson A, (2009) Effects of prenatal multimicronutrient supplementation on pregnancy outcomes: a meta-analysis. CMAJ 180: E99-108. PubMed: 19506270.
32. Mehedint MG, Craciunescu CN, Zeisel SH, (2010) Maternal dietary choline deficiency alters angiogenesis in fetal mouse hippocampus. Proc Natl Acad Sci U S A 107: 12834-12839. doi:10.1073/pnas.0914328107. PubMed: 20624989.
33. Veenema K, Solis C, Li R, Wang W, Maletz CV, et al. (2008) Adequate Intake levels of choline are sufficient for preventing elevations in serum markers of liver dysfunction in Mexican American men but are not optimal for minimizing plasma total homocysteine increases after a methionine load. Am J Clin Nutr 88: 685-692. PubMed: 18779284.
34. Zeisel SH, (2009) Importance of methyl donors during reproduction. Am J Clin Nutr 89: 673S-677S. doi:10.3945/ajcn.2008.26811D. PubMed: 19116320.
35. Maloney CA, Hay SM, Reid MD, Duncan G, Nicol F, et al. (2012) A methyl-deficient diet fed to rats during the pre- and peri-conception periods of development modifies the hepatic proteome in the adult offspring. Genes Nutr.
36. Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, et al. (2006) Maternal methyl supplements increase offspring DNA methylation at Axin Fused. Genesis 44: 401-406. doi:10.1002/dvg.20230. PubMed: 16868943.
37. Wolff GL, Kodell RL, Moore SR, Cooney CA, (1998) Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 12: 949-957. PubMed: 9707167.
38. Coupé B, Grit I, Darmaun D, Parnet P, (2009) The timing of "catch-up growth" affects metabolism and appetite regulation in male rats born with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol 297: R813-R824. doi:10.1152/ajpregu.00201.2009. PubMed: 19605764.
39. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034. PubMed: 12184808.
40. Li LC, Dahiya R, (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18: 1427-1431. doi:10.1093/bioinformatics/18.11.1427. PubMed: 12424112.
41. Stöger R, (2006) In vivo methylation patterns of the leptin promoter in human and mouse. Epigenetics 1: 155-162. doi:10.4161/epi.1.4.3400. PubMed: 17965621.
42. Melzner I, Scott V, Dorsch K, Fischer P, Wabitsch M, et al. (2002) Leptin gene expression in human preadipocytes is switched on by maturation-induced demethylation of distinct CpGs in its proximal promoter. J Biol Chem 277: 45420-45427. doi:10.1074/jbc.M208511200. PubMed: 12213831.
43. Palou M, Priego T, Sánchez J, Torrens JM, Palou A, et al. (2010) Moderate caloric restriction in lactating rats protects offspring against obesity and insulin resistance in later life. Endocrinology 151: 1030-1041. doi:10.1210/en.2009-0934. PubMed: 20068006.
44. Palou M, Torrens JM, Priego T, Sánchez J, Palou A, et al. (2011) Moderate caloric restriction in lactating rats programs their offspring for a better response to HF diet feeding in a sex-dependent manner. J Nutr Biochem 22: 574-584. doi:10.1016/j.jnutbio.2010.05.001. PubMed: 20970312.
45. Helston RM, Phillips SR, McKay JA, Jackson KA, Mathers JC, et al. (2007) Zinc transporters in the mouse placenta show a coordinated regulatory response to changes in dietary zinc intake. Placenta 28: 437-444. doi:10.1016/j.placenta.2006.07.002. PubMed: 16914197.
46. Tian X, Diaz FJ, (2013) Acute dietary zinc deficiency before conception compromises oocyte epigenetic programming and disrupts embryonic development. Dev Biol 376: 51-61. doi:10.1016/j.ydbio.2013.01.015. PubMed: 23348678.
47. Waterland RA, Jirtle RL, (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23: 5293-5300. doi:10.1128/MCB.23.15.5293-5300.2003. PubMed: 12861015.
48. Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S, (2008) Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond) 32: 1373-1379. doi:10.1038/ijo.2008.100. PubMed: 18626486.
49. Hogg K, Blair JD, von Dadelszen P, Robinson WP, (2013) Hypomethylation of the LEP gene in placenta and elevated maternal leptin concentration in early onset pre-eclampsia. Mol Cell Endocrinol 367: 64-73. doi:10.1016/j.mce.2012.12.018. PubMed: 23274423.
50. Gregoire FM, Smas CM, Sul HS, (1998) Understanding adipocyte differentiation. Physiol Rev 78: 783-809. PubMed: 9674695.
51. Bouret SG, (2010) Role of early hormonal and nutritional experiences in shaping feeding behavior and hypothalamic development. J Nutr 140: 653-657. doi:10.3945/jn.109.112433. PubMed: 20107150.
52. Sánchez J, Priego T, Palou M, Tobaruela A, Palou A, et al. (2008) Oral supplementation with physiological doses of leptin during lactation in rats improves insulin sensitivity and affects food preferences later in life. Endocrinology 149: 733-740. PubMed: 17991728.
53. Teng YW, Ellis JM, Coleman RA, Zeisel SH, (2012) Mouse betaine-homocysteine S-methyltransferase deficiency reduces body fat via increasing energy expenditure and impairing lipid synthesis and enhancing glucose oxidation in white adipose tissue. J Biol Chem 287: 16187-16198. doi:10.1074/jbc.M111.303255. PubMed: 22362777.