Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-31T23:03:44.809Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  09 March 2007

Graham C. Burdge ,
Emmanuelle Delange ,
Ludivine Dubois ,
Rebecca L. Dunn ,
Mark A. Hanson ,
Alan A. Jackson  and
Philip C. Calder
Graham C. Burdge*
Affiliation:
Institute of Human Nutrition, Biomedical Sciences Building (62), University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK
Emmanuelle Delange
Affiliation:
Institute of Human Nutrition, Biomedical Sciences Building (62), University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK
Ludivine Dubois
Affiliation:
Institute of Human Nutrition, Biomedical Sciences Building (62), University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK
Rebecca L. Dunn
Affiliation:
Institute of Human Nutrition, Biomedical Sciences Building (62), University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK
Mark A. Hanson
Affiliation:
Centre for Fetal Origins of Adult Disease, University of Southampton, Southampton, UK
Alan A. Jackson
Affiliation:
Institute of Human Nutrition, Biomedical Sciences Building (62), University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK
Philip C. Calder
Affiliation:
Institute of Human Nutrition, Biomedical Sciences Building (62), University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK
*
*Corresponding author: Dr G. C. Burdge, fax +44 23 80594383, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Reduced protein intake during pregnancy decreased maternal hepatic and plasma docosahexaenoic acid concentrations and impaired docosahexaenoic acid accumulation into fetal brain in the rat. The present study investigated whether restriction of maternal protein intake during pregnancy in the rat alters membrane phospholipid fatty acid composition in the offspring after weaning. Female rats (six per group) were mated and fed diets containing either 180 or 90 g protein/kg throughout pregnancy. Mothers were transferred to standard chow after delivery and the litters reduced to eight pups. Weaning was at 28 d and pups were killed 5 to 6 d later. Tissue weights or membrane total phosphatidylcholine (PC) and phosphatidylethanolamine (PE) concentrations in the offspring did not differ between dietary groups. There were significant differences between the 180 and 90 g/kg groups in liver, brain, lung and heart fatty acid composition that differed between tissues and phospholipid classes. For example, docosahexaenoic and arachidonic acid concentrations were 23 and 10 % lower respectively in hepatic PC, but not PE, in the 90 g/kg group. In brain, docosahexaenoic acid concentration was 17 % lower in PC, but not PE, while arachidonic acid content was 21 % greater in PE but unchanged in PC. The greatest differences were in unsaturated fatty acids, which suggests alterations to desaturase activities and/or the specificity of phospholipid biosynthesis. These results suggest that restricted maternal protein intake during pregnancy results in persistent alterations to membrane fatty acid content.

Keywords

Low-protein dietPolyunsaturated fatty acidsRatsPhospholipids
Type
Research Article
Information
British Journal of Nutrition , Volume 90 , Issue 2 , August 2003 , pp. 345 - 352
Copyright
Copyright © The Nutrition Society 2003

References

Bourre, JM, Francois, M & Youyou, A (1989) The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J Nutr 119, 1880–1892.CrossRefGoogle ScholarPubMed
Burdge, GC, Dunn, RL, Wootton, SA & Jackson, AA (2002) 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. Br J Nutr 88, 379–387.CrossRefGoogle ScholarPubMed
Burdge, GC, Hunt, AN & Postle, AD (1994) Mechanisms of hepatic phosphatidylcholine synthesis in adult rat: effects of pregnancy. Biochem J 303, 941–947.CrossRefGoogle ScholarPubMed
Burdge, GC, Kelly, FJ & Postle, A (1993 a) Mechanisms of hepatic phosphatidylcholine synthesis in the developing guinea pig: contributions of acyl remodelling and of N-methylation of phosphatidylethanolamine. Biochem J 290, 67–73.CrossRefGoogle ScholarPubMed
Burdge, GC, Kelly, FJ & Postle, AD (1993) Synthesis of phosphatidylcholine in guinea-pig fetal lung involves acyl remodelling and differential turnover of individual molecular species. Biochim Biophys Acta 1166, 251–257.CrossRefGoogle ScholarPubMed
Burdge, GC & Postle, AD (1995) Phospholipid molecular species composition of developing fetal guinea pig brain. Lipids 30, 719–724.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. Br J Nutr 84, 781–787.CrossRefGoogle ScholarPubMed
Calder, PC (2001) Polyunsaturated fatty acids, inflammation and immunity. Lipids 36, 1007–1024.CrossRefGoogle ScholarPubMed
Connor, WE & Neuringer, M (1988) The effects of n-3 fatty acid deficiency and repletion upon fatty acid composition and function of the brain and retina. Prog Clin Biol Res 282, 275–294.Google ScholarPubMed
Connor, WE, Neuringer, M & Lin, DS (1990) Dietary effects on brain fatty acid composition: the reversibility of n-3 fatty acid deficiency and turnover of docosahexaenoic acid in the brain, erythrocytes and plasma of rhesus monkeys. J Lipid Res 31, 237–247.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. J Nutr 113, 314–319.CrossRefGoogle Scholar
Folch, J, Lees, M & Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497–509.CrossRefGoogle ScholarPubMed
Heung, YM & Postle, AD (1995) The molecular selectivity of phospholipase D in HL60 granulocytes. FEBS Lett 364, 250–254.CrossRefGoogle ScholarPubMed
Innis, SM (1991) Essential fatty acids in growth and development. Prog Lipid Res 30, 39–103.CrossRefGoogle ScholarPubMed
Jackson, AA, Phillips, G, McClelland, I & Jahoor, F (2001) Synthesis of hepatic secretary proteins in normal adults consuming a diet marginally adequate in protein. Am J Physiol 281, G1179–G1187.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. J Lipid Res 6, 532–536.CrossRefGoogle Scholar
Koletzko, B & Braun, M (1991) Arachidonic acid and early human growth: is there a relation? Ann Nutr Metab 35, 128–131.CrossRefGoogle ScholarPubMed
Langley, SC & Jackson, AA (1994) Increased systolic blood pressure in adult rats induced by foetal exposure to maternal low protein diet. Clin Sci 86, 217–222.CrossRefGoogle Scholar
Langley-Evans, SC & Nwagwu, M (1998) Impaired growth and increased glucocorticoid-sensitive enzyme activities in tissues for rat fetuses exposed to maternal low protein diets. Life Sci 63, 605–615.CrossRefGoogle ScholarPubMed
Langley-Evans, SC, Whelham, SJ, Sherman, RC & Jackson, AA (1996) Weanling rats exposed to maternal low-protein diets during discrete periods of gestation exhibit differing severity of hypertension. Clin Sci 91, 607–615.CrossRefGoogle ScholarPubMed
Leaf, AA, Leighfield, MJ, Costeloe, KL & Crawford, MA (1992) Long chain polyunsaturated fatty acids and fetal growth. Early Hum Dev 30, 183–191.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. Ann Nutr Metab 30, 166–174.CrossRefGoogle ScholarPubMed
Lin, DS, Connor, WE, Anderson, GJ & Neuringer, M (1990) Effects of dietary n-3 fatty acids on the phospholipid molecular species of monkey brain. J Neurochem 55, 1200–1207.CrossRefGoogle ScholarPubMed
Litman, BJ & Mitchell, DC (1996) A role for phospholipid polyunsaturation in modulating membrane protein function. Lipids 31, Suppl., S193–S197.CrossRefGoogle ScholarPubMed
Mitchell, DC, Straume, M & Litman, BJ (1992) Role of sn-1 saturated, sn-2 polyunsaturated phospholipids in control of membrane receptor conformational equilibrium: effects of cholesterol and acyl chain unsaturation on the metarhodopsin IΦ metarhodopsin II equilibrium. Biochemistry 31, 662–670.CrossRefGoogle Scholar
Neuringer, M, Anderson, GJ & Connor, WE (1988) The essentiality of n-3 fatty acids for the development and function of the retina and brain. Annu Rev Nutr 8, 517–541.CrossRefGoogle ScholarPubMed
Neuringer, M, Connor, WE, Lin, DS, Barstad, L & Luck, S (1986) Biochemical and functional effects of prenatal and postnatal omega-3 fatty acid deficiency on retina and brain in rhesus monkeys. Proc Natl Acad Sci USA 83, 4021–4025.CrossRefGoogle ScholarPubMed
Neuringer, M, Connor, WE, Van Petten, C & Barstad, L (1984) Dietary omega-3 fatty acid deficiency and visual loss in infant rhesus monkeys. J Clin Invest 73, 272–276.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, 1337–1342.CrossRefGoogle ScholarPubMed
Pawlosky, RJ, Denkins, Y, Ward, G & Salem, N (1997) Retinal and brain accretion of long-chain polyunsaturated fatty acids in developing felines: The effects of corn oil-based maternal diets. Am J Nutr 65, 465–472.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. J Nutr 104, 894–900.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH & Fahey, GC (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123, 1939–1951.CrossRefGoogle Scholar
Reisbick, S, Neuringer, M, Hasnain, R & Connor, WE (1990) Polydipsia in rhesus monkeys deficient in omega-3 fatty acids. Physiol Behav 47, 315–323.CrossRefGoogle ScholarPubMed
Reisbick, S, Neuringer, M, Hasnain, R & Connor, WE (1994) Home cage behavior of rhesus monkeys with long-term deficiency of omega-3 fatty acids. Physiol Behav 55, 231–239.CrossRefGoogle ScholarPubMed
Ristic, V, Petrovic, G & Ristic, M (1985) Effect of a low protein diet on the serum and liver lipid content of rats. Acta Med Iugosl 39, 117–123.Google ScholarPubMed
Salem, N Jr & Niebylski, CD (1995) The nervous system has an absolute molecular species requirement for proper function. Mol Membr Biol 12, 131–134.CrossRefGoogle ScholarPubMed
Sanchez-Pinera, P, Micol, V, Corbalan-Garcia, S & Gomez-Fernandez, JC (1999) A comprehensive study of the activation of protein kinase C alpha by different diacylglycerol isomers. Biochem J 337, 387–395.CrossRefGoogle Scholar
Sinclair, AJ & Crawford, MA (1972) The accumulation of arachidonate and docosahexaenoate in the developing rat brain. J Neurochem 19, 1753–1758.CrossRefGoogle ScholarPubMed
Smit, EN, Dijkstra, JM, Schnater, TA, Seerat, E, Muskiet, FAJ & Boersma, ER (1997) Effects of malnutrition on the erythrocyte fatty acid composition and plasma vitamin E levels of Pakistani children. Acta Paediatrica 86, 690–695.CrossRefGoogle ScholarPubMed
Smit, EN, Woltil, HA, Boersma, ER & Muskkiet, FAJ (1999) Low erythrocyte docosahexaenoic acid in malnourished, often breast-fed, Pakistani infants. A matter of concern? Eur J Pediatr 158, 525CrossRefGoogle ScholarPubMed
Sprecher, H (2000) Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta 1486, 219–231.CrossRefGoogle ScholarPubMed
Su, HM, Keswick, LA & Brenna, JT (1996) Increasing dietary linolenic acid in young rats increases and then decreases docosahexaenoic acid in retina but not brain. Lipids 31, 1289–1298.CrossRefGoogle Scholar
Tijburg, LB, Samborski, RW & Vance, DE (1991) Evidence that remodeling of the fatty acids of phosphatidylcholine is regulated in isolated rat hepatocytes and involves both the sn-1 and sn-2 positions. Biochim Biophys Acta 1085, 184–190.CrossRefGoogle ScholarPubMed
Weisinger, HS, Armitage, JA, Sinclair, AJ, Vingrys, AJ, Burns, PL & Weisinger, RS (2001) Perinatal omega-3 fatty acid deficiency affects blood pressure later in life. Nat Med 7, 258–259.CrossRefGoogle ScholarPubMed