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Effect of reduced dietary protein intake on hepatic and plasma essential fatty acid concentrations in the adult female rat: effect of pregnancy and consequences for accumulation of arachidonic and docosahexaenoic acids in fetal liver and brain*

Published online by Cambridge University Press:  09 March 2007

Graham C. Burdge*
Affiliation:
Institute of Human Nutrition, University of Southampton, Hants., UK
Rebecca L. Dunn
Affiliation:
Institute of Human Nutrition, University of Southampton, Hants., UK
Stephen A. Wootton
Affiliation:
Institute of Human Nutrition, University of Southampton, Hants., UK
Alan A. Jackson
Affiliation:
Institute of Human Nutrition, University of Southampton, Hants., UK
*
Corresponding author: Dr G. C. Burdge, fax +44 23 80794945, email G.C.Burdge@soton.ac.uk
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Abstract

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During pregnancy, the accumulation of long-chain polyunsaturated fatty acids (LCPUFA) in fetal tissues places a substantial demand upon maternal lipid metabolism. As lipid metabolism is intimately linked to aspects of protein metabolism, a reduced protein intake in pregnancy may impair activities of enzymes and transport proteins responsible for supplying LCPUFA to the fetus, thereby compromising fetal development. We have investigated the effect of reduced protein intake on LCPUFA status in the non-pregnant rat and in the pregnant rat, and in fetus at day 20 of gestation. Female rats (n 5 per group) were either mated and fed the control diet (180 g protein/kg) or low-protein diet (90 g protein/kg, LPD) diet throughout pregnancy, or fed the control diet or LPD for 20 d (non-pregnant animals). The fatty acid compositions of maternal liver and plasma, and fetal liver and brain were determined by GC. Feeding the LPD did not lead to any gross changes either in adult or fetal growth, or in total lipid concentrations in adult rat liver. However, the LPD was associated specifically with lower liver (42·6 %) and plasma (19·4 %) phosphatidylcholine (PC), and plasma triacylglycerol (28·6 %) docosahexaenoic acid (DHA) concentrations in pregnant rats and reduced fetal brain PC- (26·1 %) and phosphatidylethanolamine- (25·6 %) DHA concentrations. Together, these results show that variations in maternal dietary protein consumption alter DHA status in pregnancy and modify DHA accumulation into the fetal brain. The present results suggest that lower maternal protein intakes reduce delivery of DHA from the mother to the fetus, which may impair development and function of the fetal brain.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2002

References

Burdge, GC, Hunt, AN & Postle, AD (1994) Mechanisms of hepatic phosphatidylcholine synthesis in adult rat: effects of pregnancy. Biochemical Journal 303, 941947.CrossRefGoogle ScholarPubMed
Burdge, GC & Postle, AD (1994) Hepatic phospholipid molecular species in the guinea pig. Adaptations to pregnancy. Lipids 29, 259264.CrossRefGoogle Scholar
Burdge, GC & Postle, AD (1995 a) Phospholipid molecular species composition of developing fetal guinea pig brain. Lipids 30, 719724.CrossRefGoogle ScholarPubMed
Burdge, GC & Postle, AD (1995 b) Effect of maternal ethanol consumption during pregnancy on the phospholipid molecular species composition of fetal guinea-pig brain, liver and plasma. Biochimica et Biophysica Acta 1256, 346352.CrossRefGoogle ScholarPubMed
Burdge, GC, Wright, P, Jones, AE & Wootton, SA (2000) A method for separation of phosphatidylcholine, triacylglycerol, non-esterified fatty acids and cholesterol esters from plasma by solid-phase extraction. British Journal of Nutrition 84, 781787.CrossRefGoogle ScholarPubMed
Carnielli, VP, Wattimena, DJL, Luijendijk, IHT, Boerlage, HJ & Sauer, PJJ (1996) The very low birth weight premature infant is capable of synthesizing arachidonic and docosahexaenoic acid from linoleic and linolenic acid. Pediatric Research 40, 169174.CrossRefGoogle Scholar
Chambaz, J, Ravel, D, Manier, MC, Pepin, D, Mulliez, N & Bereziat, G (1985) Essential fatty acid interconversion in the human liver. Biology of the Neonate 47, 136140.CrossRefGoogle Scholar
Chen, Z-Y, Yang, J & Cunnane, SC (1992) Gestational hyperlipidaemia in the rat is characterised by accumulation of n−6 and n−3 fatty acids, especially docosahexaenoic acid. Biochimica et Biophysical Acta 1127, 263269.CrossRefGoogle ScholarPubMed
Clandinin, MT, Chapell, JE, Leong, S, Heim, T, Swyer, PR & Chance, GW (1980 a) Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Human Development 4, 121129.CrossRefGoogle ScholarPubMed
Clandinin, MT, Chapell, JE, Leong, S, Heim, T, Swyer, PR & Chance, GW (1980) Extrauterine fatty acid accretion in infant brain: implications for fatty acid requirements. Early Human Development 4, 131138.CrossRefGoogle ScholarPubMed
Connor, WE, Neuringer, M & Lin, DS (1990) Dietary effects on brain fatty acid composition: the reversibility of n−3 deficiency and turnover of docosahexaenoic acid in the brain, erythrocytes and plasma of rhesus monkeys. Journal of Lipid Research 31, 237247.CrossRefGoogle ScholarPubMed
Crawford, MA, Hassam, AG, Hall, BM & Williams, G (1976) Essential fatty acids and fetal brain growth. Lancet 1, 452453.CrossRefGoogle ScholarPubMed
De Thomas, ME, Mercuri, O & Serres, C (1983) Effect of cross-fostering rats at birth on the normal supply of essential fatty acids during protein deficiency. Journal of Nutrition 113, 314319.CrossRefGoogle Scholar
Demmelmair, H, v. Schenck, U, Behrendt, E, Sauerwald, T & Koletzko, B (1995) Estimation of arachidonic acid synthesis in full term neonates using natural variation of 13C content. Journal of Pediatric Gastroenterology and Nutrition 21, 3136.Google ScholarPubMed
Dobbing, J & Sands, J (1979) Comparative aspects of the brain growth spurt. Early Human Development 3, 7983.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497509.CrossRefGoogle ScholarPubMed
Innis, SM (1991) Essential fatty acids in growth and development. Progress in Lipid Research 30, 39103.CrossRefGoogle ScholarPubMed
Jackson, AA, Philips, G, McClelland, I & Jahoor, F (2001) Synthesis of hepatic secretary proteins in normal adults consuming a diet marginally adequate in protein. American Journal of Physiology 281, G1179G1187.Google Scholar
Kishimoto, Y, Davies, WE & Radin, NS (1965) Developing rat brain: changes in cholesterol, galactolipids, and the individual fatty acids of gangliosides and glycerophosphotidates. Journal of Lipid Research 6, 532536.CrossRefGoogle Scholar
Koletzko, B & Braun, M (1991) Arachidonic acid and early human growth: Is there a relation. Annals of Nutrition and Metabolism 35, 128131.CrossRefGoogle ScholarPubMed
Langley, SC & Jackson, AA (1994) Increased systolic blood pressure in adult rats induced by foetal exposure to maternal low protein diet. Clinical Science 86, 217222.CrossRefGoogle Scholar
Langley-Evans, SC, Clamp, AG, Grimble, RF & Jackson, AA (1996) Influence of dietary fats upon systolic blood pressure in the rat. International Journal of Food Sciences and Nutrition 47, 417425.CrossRefGoogle ScholarPubMed
Langley-Evans, SC, Sherman, RL, Welham, SJM, Nwagwu, MO, Gardiner, DS & Jackson, AA (1999) Intrauterine programming of hypertension: the role of the renin–angiotensin system. Biochemical Society Transactions 27, 8893.CrossRefGoogle ScholarPubMed
Leaf, AA, Leighfield, MJ, Costeloe, KL & Crawford, MA (1992) Long chain polyunsaturated fatty acids and fetal growth. Early Human Development 30, 183191.CrossRefGoogle ScholarPubMed
Leat, WMF, Curtis, R, Millicham, NJ & Cox, RW (1986) Retinal function in rats and guinea-pigs reared on diets low in essential fatty acids and supplemented with linoleic or linolenic acids. Annals of Nutrition and Metabolism 30, 166174.CrossRefGoogle ScholarPubMed
Li, Z, Kaplan, ML & Hatchey, DL (2000) Hepatic microsomal and peroxisomal docosahexaenoate biosynthesis during piglet development. Lipids 35, 13251333.CrossRefGoogle ScholarPubMed
Marin, MC, De Thomas, ME, Serres, C & Mercuri, O (1995) Protein–energy malnutrition during gestation and lactation in rats affects growth rate, brain development and essential fatty acid metabolism. Journal of Nutrition 125, 10171024.Google ScholarPubMed
Neuringer, M, Anderson, GJ & Connor, WE (1988) The essentiality of n−3 fatty acids for the development and function of the retina and brain. Annual Review of Nutrition 8, 517541.CrossRefGoogle ScholarPubMed
Neuringer, M, Connor, WE, Van Petten, C & Barstrad, L (1984) Dietary omega-3 fatty acid deficiency and visual loss in infant rhesus monkeys. Journal of Clinical Investigation 73, 272276.CrossRefGoogle ScholarPubMed
Otto, SJ, Van Houwelingen, AC, Manninen, A, Godfrey, K, Lopez-Jaramillo, P & Hornstra, G (1997) Maternal and neonatal essential fatty acid status in phospholipids: an international comparative study. European Journal of Clinical Nutrition 51, 232242.CrossRefGoogle ScholarPubMed
Ozanne, SE, Martinsz, ND, Petry, CJ, Loizou, CL & Hales, CN (1998) Maternal low protein diet in rats programmes fatty acids desaturase activities in the offspring. Diabetologica 41, 13371342.CrossRefGoogle ScholarPubMed
Peluffo, RO & Brenner, RR (1974) Influence of dietary protein on 6- and 9-desaturation of fatty acids in rats of different ages and in different seasons. Journal of Nutrition 104, 894900.CrossRefGoogle ScholarPubMed
Postle, AD, Al, MDM, Burdge, GC & Hornstra, G (1995) The composition of individual molecular species of plasma phosphatidylcholine in human pregnancy. Early Human Development 43, 4758.CrossRefGoogle ScholarPubMed
Reisbick, S, Neuringer, M, Hasnain, R & Connor, WE (1990) Polydipsia in rhesus monkeys deficient in omega-3 fatty acids. Physiology of Behaviour 47, 315323.CrossRefGoogle ScholarPubMed
Reisbick, S, Neuringer, M, Hasnain, R & Connor, WE (1994) Home cage behaviour of rhesus monkeys with long-term deficieny of omega-3 fatty acids. Physiology of Behaviour 55, 231239.CrossRefGoogle Scholar
Ristic, V, Petrovic, G & Ristic, M (1985) Effect of a low protein diet on the serum and liver lipid content of rats. Acta Medica Iugoslavica 39, 117123.Google ScholarPubMed
Salem, N & Niebylski, CD (1995) The nervous system has an absolute molecular species requirement for proper function. Molecular Membrane Biology 12, 131134.CrossRefGoogle ScholarPubMed
Salem, N, Wegher, B, Mena, P & Uauy, R (1996) Arachidonic and docosahexaenoic acids are biosynthesised from their 18-carbon precursors in human infants. Proceedings of the National Academy of Sciences USA 93, 4954.CrossRefGoogle Scholar
Sanders, TAB & Rana, SK (1987) Comparison of the metabolism of linoleic and linolenic acids in the fetal rat. Annals of Nutrition and Metabolism 31, 349353.CrossRefGoogle Scholar
Sauerwald, TU, Hachey, DL, Jensen, CL, Chen, H, Anderson, RE & Heird, WC (1997) Intermediates in endogenous synthesis of C22: 6 ω3 and C20: 4 ω6 by term and preterm infants. Pediatric Research 41, 183187.CrossRefGoogle Scholar
Sinclair, AJ & Crawford, MA (1972) The accumulation of arachidonate and docosahexaenoate in the developing rat brain. Journal of Neurochemistry 19, 17531758.CrossRefGoogle ScholarPubMed
Sprecher, H, Chen, Q & Yin, FQ (1999) Regulation of the biosynthesis of 22: 5 n−6 and 22: 6 n−3 – a complex intracellular process. Lipids 34, 153156.CrossRefGoogle Scholar
Su, HM, Bernardo, L, Mirmiran, M, Ma, XH, Corso, TN, Nathanielsz, PW & Brenna, JT (1999) Bioequivalence of dietary alpha-linolenic and docosahexaenoic acids as sources of docosahexaenoate accretion in brain and associated organs of neonatal baboons. Pediatric Research 45, 8793.CrossRefGoogle ScholarPubMed
Su, HM, Bernardo, L, Mirmiran, M, Ma, XH, Nathanielsz, PW & Brenna, JT (1999) Dietary 18: 3 n−3 and 22: 6 n−3 as sources of 22: 6 n−3 accretion in neonatal baboon brain and associated organs. Lipids 34, Suppl., S347S350.CrossRefGoogle ScholarPubMed
Uauy, RD, Birch, DG, Birch, EE, Tyson, JE & Hoffman, DR (1990) Effect of dietary omega-3 fatty acids on retinal function of very-low-birth-weight neonates. Pediatric Research 28, 485492.CrossRefGoogle ScholarPubMed