High vitamin intake by Wistar rats during pregnancy alters tissue fatty acid concentration in the offspring fed an obesogenic diet

Metabolism: Clinical and Experimental

Volumn 58, Issue 5, 2009, Pages 722-730

  Reza López, Sandra A ^a   Anderson, G Harvey ^a   Szeto, Ignatius M Y ^a   Taha, Ameer Y ^a   Ma, David W L ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; FATTY ACID; LIPID; MONOUNSATURATED FATTY ACID; OLEIC ACID; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHOLIPID; STEARIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRTH; BRAIN; CONTROLLED STUDY; FAT BODY; FEMALE; GAS CHROMATOGRAPHY; LIPID LIVER LEVEL; LIPID METABOLISM; LIVER; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGENY; QUADRICEPS FEMORIS MUSCLE; RAT; VITAMIN INTAKE; WEANING;

ADIPOSE TISSUE; ANIMALS; BRAIN; FATTY ACIDS; FEMALE; LIVER; LONGITUDINAL STUDIES; MALE; MUSCLE, SKELETAL; OBESITY; PREGNANCY; RANDOM ALLOCATION; RATS; RATS, WISTAR; VITAMINS;

EID: 64549125603     PISSN: 00260495     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.metabol.2009.01.014     Document Type: Article

References (71)

1. Krauss-Etschmann S., Shadid R., Campoy C., et al. Effects of fish-oil and folate supplementation of pregnant women on maternal and fetal plasma concentrations of docosahexaenoic acid and eicosapentaenoic acid: a European randomized multicenter trial. Am J Clin Nutr 85 (2007) 1392-1400
2. Friesen R., and Innis S.M. Maternal dietary fat alters amniotic fluid and fetal intestinal membrane essential n-6 and n-3 fatty acids in the rat. Am J Physiol Gastrointest Liver Physiol 290 (2006) G505-G510
3. Amusquivar E., and Herrera E. Influence of changes in dietary fatty acids during pregnancy on placental and fetal fatty acid profile in the rat. Biol Neonate 83 (2003) 136-145
4. Armitage J.A., Lakasing L., Taylor P.D., et al. Developmental programming of aortic and renal structure in offspring of rats fed fat-rich diets in pregnancy. J Physiol 565 (2005) 171-184
5. Ghosh P., Bitsanis D., Ghebremeskel K., Crawford M.A., and Poston L. Abnormal aortic fatty acid composition and small artery function in offspring of rats fed a high fat diet in pregnancy. J Physiol 533 (2001) 815-822
6. Buckley A.J., Keseru B., Briody J., Thompson M., Ozanne S.E., and Thompson C.H. Altered body composition and metabolism in the male offspring of high fat-fed rats. Metabolism 54 (2005) 500-507
7. Levant B., Ozias M.K., Jones K.A., and Carlson S.E. Differential effects of modulation of docosahexaenoic acid content during development in specific regions of rat brain. Lipids 41 (2006) 407-414
8. Innis S.M. Essential fatty acid transfer and fetal development. Placenta 26 Suppl A (2005) S70-S75
9. Otto S.J., van Houwelingen A.C., Badart-Smook A., and Hornstra G. Changes in the maternal essential fatty acid profile during early pregnancy and the relation of the profile to diet. Am J Clin Nutr 73 (2001) 302-307
10. Hornstra G., Al M.D., van Houwelingen A.C., and Foreman-van Drongelen M.M. Essential fatty acids in pregnancy and early human development. Eur J Obstet Gynecol Reprod Biol 61 (1995) 57-62
11. Al M.D., van Houwelingen A.C., Kester A.D., Hasaart T.H., de Jong A.E., and Hornstra G. Maternal essential fatty acid patterns during normal pregnancy and their relationship to the neonatal essential fatty acid status. Br J Nutr 74 (1995) 55-68
12. Marin M.C., De Tomas M.E., Serres C., and Mercuri O. Protein-energy malnutrition during gestation and lactation in rats affects growth rate, brain development and essential fatty acid metabolism. J Nutr 125 (1995) 1017-1024
13. Burdge G.C., Delange E., Dubois L., et al. Effect of reduced maternal protein intake in pregnancy in the rat on the fatty acid composition of brain, liver, plasma, heart and lung phospholipids of the offspring after weaning. Br J Nutr 90 (2003) 345-352
14. Ozanne S.E., Martensz N.D., Petry C.J., Loizou C.L., and Hales C.N. Maternal low protein diet in rats programmes fatty acid desaturase activities in the offspring. Diabetologia 41 (1998) 1337-1342
15. Wolff G.L., Kodell R.L., Moore S.R., and Cooney C.A. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 12 (1998) 949-957
16. Maloney C.A., and Rees W.D. Gene-nutrient interactions during fetal development. Reproduction 130 (2005) 401-410
17. Desvergne B., Michalik L., and Wahli W. Transcriptional regulation of metabolism. Physiol Rev 86 (2006) 465-514
18. Ziouzenkova O., and Plutzky J. Retinoid metabolism and nuclear receptor responses: new insights into coordinated regulation of the PPAR-RXR complex. FEBS Lett 582 (2008) 32-38
19. Lillycrop K.A., Phillips E.S., Jackson A.A., Hanson M.A., and Burdge G.C. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135 (2005) 1382-1386
20. Burdge G.C., Hanson M.A., Slater-Jefferies J.L., and Lillycrop K.A. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life?. Br J Nutr 97 (2007) 1036-1046
21. Despret S., Dinh L., Clement M., and Bourre J.M. Alteration of delta-6 desaturase by vitamin E in rat brain and liver. Neurosci Lett 145 (1992) 19-22
22. Tsuge H., Hotta N., and Hayakawa T. Effects of vitamin B-6 on (n-3) polyunsaturated fatty acid metabolism. J Nutr 130 (2000) 333S-334S
23. Szeto I.M., Aziz A., Das P.J., et al. High multivitamin intake by Wistar rats during pregnancy results in increased food intake and components of the metabolic syndrome in male offspring. Am J Physiol Regul Integr Comp Physiol 295 (2008) R575-R582
24. Reeves P.G. Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr 127 (1997) 838S-841S
25. Petry C.J., Ozanne S.E., Wang C.L., and Hales C.N. Early protein restriction and obesity independently induce hypertension in 1-year-old rats. Clin Sci (Lond) 93 (1997) 147-152
26. Folch J., Lees M., and Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226 (1957) 497-509
27. Andersson A., Nalsen C., Tengblad S., and Vessby B. Fatty acid composition of skeletal muscle reflects dietary fat composition in humans. Am J Clin Nutr 76 (2002) 1222-1229
28. Spector A.A., and Yorek M.A. Membrane lipid composition and cellular function. J Lipid Res 26 (1985) 1015-1035
29. Aas V., Rokling-Andersen M.H., Kase E.T., Thoresen G.H., and Rustan A.C. Eicosapentaenoic acid (20:5 n-3) increases fatty acid and glucose uptake in cultured human skeletal muscle cells. J Lipid Res 47 (2006) 366-374
30. Hulbert A.J., Turner N., Storlien L.H., and Else P.L. Dietary fats and membrane function: implications for metabolism and disease. Biol Rev Camb Philos Soc 80 (2005) 155-169
31. Borkman M., Storlien L.H., Pan D.A., Jenkins A.B., Chisholm D.J., and Campbell L.V. The relation between insulin sensitivity and the fatty-acid composition of skeletal-muscle phospholipids. N Engl J Med 328 (1993) 238-244
32. Pan D.A., Hulbert A.J., and Storlien L.H. Dietary fats, membrane phospholipids and obesity. J Nutr 124 (1994) 1555-1565
33. Pan D.A., Lillioja S., Milner M.R., et al. Skeletal muscle membrane lipid composition is related to adiposity and insulin action. J Clin Invest 96 (1995) 2802-2808
34. Ghafoorunissa, Ibrahim A., Rajkumar L., and Acharya V. Dietary (n-3) long chain polyunsaturated fatty acids prevent sucrose-induced insulin resistance in rats. J Nutr 135 (2005) 2634-2638
35. Rees W.D., McNeil C.J., and Maloney C.A. The roles of PPARs in the fetal origins of metabolic health and disease. PPAR Res 2008 (2008) 459030
36. Waterland R.A. Do maternal methyl supplements in mice affect DNA methylation of offspring?. J Nutr 133 (2003) 238
37. Waterland R.A., and Jirtle R.L. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20 (2004) 63-68
38. Waterland R.A., and Jirtle R.L. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23 (2003) 5293-5300
39. Smith A.G., and Muscat G.E. Skeletal muscle and nuclear hormone receptors: implications for cardiovascular and metabolic disease. Int J Biochem Cell Biol 37 (2005) 2047-2063
40. Ozias M.K., and Schalinske K.L. All-trans-retinoic acid rapidly induces glycine N-methyltransferase in a dose-dependent manner and reduces circulating methionine and homocysteine levels in rats. J Nutr 133 (2003) 4090-4094
41. Kapoor A., Petropoulos S., and Matthews S.G. Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Res Rev 57 (2008) 586-595
42. Wilcoxon J.S., and Redei E.E. Maternal glucocorticoid deficit affects hypothalamic-pituitary-adrenal function and behavior of rat offspring. Horm Behav 51 (2007) 321-327
43. Holmes M.C., Abrahamsen C.T., French K.L., Paterson J.M., Mullins J.J., and Seckl J.R. The mother or the fetus? 11beta-Hydroxysteroid dehydrogenase type 2 null mice provide evidence for direct fetal programming of behavior by endogenous glucocorticoids. J Neurosci 26 (2006) 3840-3844
44. Kapoor A., Dunn E., Kostaki A., Andrews M.H., and Matthews S.G. Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Physiol 572 (2006) 31-44
45. Beneke S., and Rooney S.A. Glucocorticoids regulate expression of the fatty acid synthase gene in fetal rat type II cells. Biochim Biophys Acta 1534 (2001) 56-63
46. Cleasby M.E., Kelly P.A., Walker B.R., and Seckl J.R. Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids. Endocrinology 144 (2003) 999-1007
47. Rao S., Joshi S., Kale A., Hegde M., and Mahadik S. Maternal folic acid supplementation to dams on marginal protein level alters brain fatty acid levels of their adult offspring. Metabolism 55 (2006) 628-634
48. Burdge G.C., Slater-Jefferies J.L., Grant R.A., et al. Sex, but not maternal protein or folic acid intake, determines the fatty acid composition of hepatic phospholipids, but not of triacylglycerol, in adult rats. Prostaglandins Leukot Essent Fatty Acids 78 (2008) 73-79
49. Childs C.E., Romeu-Nadal M., Burdge G.C., and Calder P.C. Gender differences in the n-3 fatty acid content of tissues. Proc Nutr Soc 67 (2008) 19-27
50. Jalouli M., Carlsson L., Ameen C., et al. Sex difference in hepatic peroxisome proliferators activated receptor alpha expression: influence of pituitary and gonadal hormones. Endocrinology 144 (2003) 101-109
51. Luxon B.A., Holly D.C., Milliano M.T., and Weisiger R.A. Sex differences in multiple steps in hepatic transport of palmitate support a balanced uptake mechanism. Am J Physiol 274 (1998) G52-G61
52. Luxon B.A., and Weisiger R.A. Sex differences in intracellular fatty acid transport: role of cytoplasmic binding proteins. Am J Physiol 265 (1993) G831-G841
53. Sorrentino D., Zhou S.L., Kokkotou E., and Berk P.D. Sex differences in hepatic fatty acid uptake reflect a greater affinity of the transport system in females. Am J Physiol 263 (1992) G380-G385
54. de Heredia F.P., Larque E., Portillo M.D., Canteras M., Zamora S., and Garaulet M. Age-related changes in fatty acids from different adipose depots in rat and their association with adiposity and insulin. Nutrition 24 (2008) 1013-1022
55. Tamburini I., Quartacci M.F., Izzo R., and Bergamini E. Effects of dietary restriction on age related changes in the phospholipid fatty acid composition of various rat tissues. Aging Clin Exp Res 16 (2004) 425-431
56. Erhuma A., Bellinger L., Langley-Evans S.C., and Bennett A.J. Prenatal exposure to undernutrition and programming of responses to high-fat feeding in the rat. Br J Nutr 98 (2007) 517-524
57. Haugaard S.B., Madsbad S., Hoy C.E., and Vaag A. Dietary intervention increases n-3 long chain polyunsaturated fatty acids in skeletal muscle membrane phospholipids of obese subjects. Implications for insulin sensitivity. Clin Endocrinol (Oxf) 64 (2006) 169-178
58. Ghafoorunissa, Ibrahim A., and Natarajan S. Substituting dietary linoleic acid with alpha linolenic acid improves insulin sensitivity in sucrose fed rats. Biochim Biophys Acta 1733 (2005) 67-75
59. Clore J.N., Li J., Gill R., et al. Skeletal muscle phosphatidylcholine fatty acids and insulin sensitivity in normal humans. Am J Physiol 275 (1998) E665-E670
60. Kaduce T.L., Chen Y., Hell J.W., and Spector A.A. Docosahexaenoic acid synthesis from n-3 fatty acid precursors in rat hippocampal neurons. J Neurochem 105 (2008) 1525-1535
61. Rapoport S.I., Rao J.S., and Igarashi M. Brain metabolism of nutritionally essential polyunsaturated fatty acids depends on both the diet and the liver. Prostaglandins Leukot Essent Fatty Acids 77 (2007) 251-261
62. Coti B.P., O'Kusky J.R., and Innis S.M. Maternal dietary (n-3) fatty acid deficiency alters neurogenesis in the embryonic rat brain. J Nutr 136 (2006) 1570-1575
63. Uauy R., and Dangour A.D. Nutrition in brain development and aging: role of essential fatty acids. Nutr Rev 64 (2006) S24-S33
64. Innis S.M. The role of dietary n-6 and n-3 fatty acids in the developing brain. Dev Neurosci 22 (2000) 474-480
65. Lagiou P., Mucci L., Tamimi R., et al. Micronutrient intake during pregnancy in relation to birth size. Eur J Nutr 44 (2005) 52-59
66. Yajnik C.S., Deshpande S.S., Jackson A.A., et al. Vitamin B(12) and folate concentrations during pregnancy and insulin resistance in the offspring: the Pune Maternal Nutrition Study. Diabetologia 51 (2008) 29-38
67. Gluckman P.D., Hanson M.A., and Spencer H.G. Predictive adaptive responses and human evolution. Trends Ecol Evol 20 (2005) 527-533
68. Subcommittee on Laboratory Animal Nutrition, Committee on Animal Nutrition, Board on Agriculture, National Research Council. Nutrient requirements of laboratory animals (1995), National Academy Press, Washington, DC
69. Okano J., Suzuki S., and Shiota K. Involvement of apoptotic cell death and cell cycle perturbation in retinoic acid-induced cleft palate in mice. Toxicol Appl Pharmacol 221 (2007) 42-56
70. Colakoglu N., Kukner2 A., Oner J., Sonmez M.F., Oner H., and Ozan E. Effects of high dose retinoic acid on TGF-b2 expression during pancreatic organogenesis. J Molec Histol 36 (2005) 413-418
71. Achon M., Alonso-Aperte E., Reyes L., Ubeda N., and Varela-Moreiras G. High-dose folic acid supplementation in rats: effects on gestation and the methionine cycle. Br J Nutr 83 (2000) 177-183