Abstract
Purpose
The utilization of long-chain polyunsaturated fatty acids (LCPUFA) by the fetus may exceed its capacity to synthesize them from essential fatty acids, so they have to come from the mother. Since adipose tissue lipolytic activity is greatly accelerated under fasting conditions during late pregnancy, the aim was to determine how 24 h fasting in late pregnant rats given diets with different fatty acid compositions affects maternal and fetal tissue fatty acid profiles.
Methods
Pregnant Sprague–Dawley rats were given isoenergetic diets containing 10% palm-, sunflower-, olive- or fish-oil. Half the rats were fasted from day 19 of pregnancy and all were studied on day 20. Triacylglycerols (TAG), glycerol and non-esterified fatty acids (NEFA) were analyzed by enzymatic methods and fatty acid profiles were analyzed by gas chromatography.
Results
Fasting caused increments in maternal plasma NEFA, glycerol and TAG, indicating increased adipose tissue lipolytic activity. Maternal adipose fatty acid profiles paralleled the respective diets and, with the exception of animals on the olive oil diet, maternal fasting increased the plasma concentration of most fatty acids. This maintains the availability of LCPUFA to the fetus during brain development.
Conclusions
The results show the major role played by maternal adipose tissue in the storage of dietary fatty acids during pregnancy, thus ensuring adequate availability of LCPUFA to the fetus during late pregnancy, even when food supply is restricted.
Similar content being viewed by others
Notes
Salt mix (g/kg diet): copper sulfate 0.1; ammonium molybdate 0.026; sodium iodate 0.000310; potassium chromate 0.028; zinc sulfate 0.091; calcium hydrogen phosphate 0.145; ammonium ferrous sulfate 2.228; magnesium sulfate 3.37; manganese sulfate 1.125; sodium chloride 4; calcium carbonate 9.89; potassium dihydrogen phosphate 14.75).
Vitamin mix (mg/kg diet): retinyl palmitate 2.4; cholecalciferol 0.025; menadione sodium bisulfite 0.8; biotin 0.22; cyanocobalamin 0.01; riboflavim 6.6; thiamin hydrochloride 6.6; α-tocopherol acetate 100.
References
Awad AB (1981) Effect of dietary lipids on composition and glucose utilization by rat adipose tissue. JNutr 111:34–39
Becker W, Bruce A (1986) Retention of linoleic acid in carcass lipids of rats fed different levels of essential fatty acids. Lipids 21:121–126
Nelson GJ, Kelley DS, Schmidt PC, Serrato SM (1987) The influence of dietary fat on the lipogenic activity and fatty acid composition of rat adipose tissue. Lipids 22:338–344
Sanchez-Blanco C, Amusquivar E, Bispo K, Herrera E (2016) Influence of cafeteria diet and fish oil in pregnancy and lactation on pups’ body weight and fatty acid profiles in rats. Eur J Nutr 55:1741–1753
Anderson DB, Kauffman RG (1973) Cellular and enzymatic changes in porcine adipose tissue during growth. J Lipid Res 14:160–168
Etherton TD, Allen CE (1980) Effects of age and adipocyte size on glucose and palmitate metabolism and oxidation in pigs. J Anim Sci 50:1073–1084
Gandemer G, Pascal G, Durand G (1985) Comparative changes in the lipogenic enzyme activities and in the in vivo fatty acid synthesis in liver and adipose tissues during the post-weaning growth of male rats. Comp Biochem Physiol B 82:581–586
Baylin A, Kabagambe EK, Siles X, Campos H (2002) Adipose tissue biomarkers of fatty acid intake. Am J Clin Nutr 76:750–757
Leaf DA, Connor WE, Barstad L, Sexton G (1995) Incorporation of dietary n-3 fatty acids into the fatty acids of human adipose tissue and plasma lipid classes. Am J Clin Nutr 62:68–73
Lhuillery C, Mebarki S, Lecourtier MJ, Demarne Y (1988) Influence of different dietary fats on the incorporation of exogenous fatty acids into rat adipose glycerides. J Nutr 118:1447–1454
Weber N, Klein E, Mukherjee KD (2002) The composition of the major molecular species of adipose tissue triacylglycerols of rats reflects those of dietary rapeseed, olive and sunflower oils. J Nutr 132:726–732
Amusquivar E, Herrera E (2003) Influence of changes in dietary fatty acids during pregnancy on placental and fetal fatty acid profile in the rat. Biol Neonate 83:136–145
Herrera E (2002) Lipid metabolism in pregnancy and its consequences in the fetus and newborn. Endocr 19:43–55
Herrera E, Ortega-Senovilla H (2014) Lipid metabolism during pregnancy and its implications for fetal growth. Curr Pharm Biotechnol 15:24–31
Herrera E, Desoye G (2016) Maternal and fetal lipid metabolism under normal and gestational diabetic conditions. Horm Mol Biol Clin Investig 26:109–127
Herrera E, Lasunción MA, Martín A, Zorzano A (1992) Carbohydrate-lipid interactions in pregnancy. In: Herrera E, Knopp RH (eds) Perinatal biochemistry. CRC Press, Boca Raton, pp 1–18
Knopp RH, Boroush MA, O’Sullivan JB (1975) Lipid metabolism in pregnancy. II. Postheparin lipolytic acitivity and hypertriglyceridemia in the pregnant rat. Metabolism 24:481–493
Alvarez JJ, Montelongo A, Iglesias A, Lasuncion MA, Herrera E (1996) Longitudinal study on lipoprotein profile, high density lipoprotein subclass, and postheparin lipases during gestation in women. J Lipid Res 37:299–308
Martin-Hidalgo A, Holm C, Belfrage P, Schotz MC, Herrera E (1994) Lipoprotein lipase and hormone-sensitive lipase activity and mRNA in rat adipose tissue during pregnancy. Am J Physiol 266:E930–E935
Moore BJ, Brasel JA (1984) One cycle of reproduction consisting of pregnancy, lactation or no lactation, and recovery: effects on fat pad cellularity in ad libitum-fed and food-restricted rats. J Nutr 114:1560–1565
Murphy SP, Abrams BF (1993) Changes in energy intakes during pregnancy and lactation in a national sample of US women. Am J Public Health 83:1161–1163
Piers LS, Diggavi SN, Thangam S, van Raaij JM, Shetty PS, Hautvast JG (1995) Changes in energy expenditure, anthropometry, and energy intake during the course of pregnancy and lactation in well-nourished Indian women. Am J Clin Nutr 61:501–513
Hamosh M, Clary TR, Chernick SS, Scow RO (1970) Lipoprotein lipase activity of adipose and mammary tissue and plasma triglyceride in pregnant and lactating rats. Biochim Biophys Acta 210:473–482
Herrera E, Lasuncion MA, Gomez-Coronado D, Aranda P, Lopez-Luna P, Maier I (1988) Role of lipoprotein lipase activity on lipoprotein metabolism and the fate of circulating triglycerides in pregnancy. Am J Obstet Gynecol 158:1575–1583
Ramirez I, Llobera M, Herrera E (1983) Circulating triacylglycerols, lipoproteins, and tissue lipoprotein lipase activities in rat mothers and offspring during the perinatal period: effect of postmaturity. Metabolism 32:333–341
Elliott JA (1975) The effect of pregnancy on the control of lipolysis in fat cells isolated from human adipose tissue. Eur J Clin Invest 5:159–163
Knopp RH, Herrera E, Freinkel N (1970) Carbohydrate metabolism in pregnancy. 8. Metabolism of adipose tissue isolated from fed and fasted pregnant rats during late gestation. J Clin Invest 49:1438–1446
Williams C, Coltart TM (1978) Adipose tissue metabolism in pregnancy: the lipolytic effect of human placental lactogen. Br J Obstet Gynaecol 85:43–46
Herrera E, Lasunción MA (2017) Maternal-fetal tranfer of lipid metabolites. In: Polin RA, Abman SH, Rowitch DH, Benitz WE, Fox WW (eds) Fetal and neonatal physiology. Elsevier, Philadelphia, pp 342–353
Mampel T, Villarroya F, Herrera E (1985) Hepatectomy-nephrectomy effects in the pregnant rat and fetus. Biochem Biophys Res Commun 131:1219–1225
Ramos P, Herrera E (1995) Reversion of insulin resistance in the rat during late pregnancy by 72-h glucose infusion. Am J Physiol 269:E858-E863
Knopp RH, Bonet B, Lasunción MA, Montelongo A, Herrera E (1992) Lipoprotein metabolism in pregnancy. In: Herrera E, Knopp RH (eds) Perinatal biochemistry. CRC Press, Boca Raton, pp 19–51
Herrera E, Ortega-Senovilla H (2016) The roles of fatty acids in fetal development. In: Duttaroy AK, Basak S (eds) Human placental trophoblkasts impact of maternal nutrition. CRC Press, Boca Raton, pp 93–111
Fernandes FS, Tavares do Carmo M, Herrera E (2012) Influence of maternal diet during early pregnancy on the fatty acid profile in the fetus at late pregnancy in rats. Lipids 47:505–517
Crawford MA, Hassam AG, Stevens PA (1981) Essential fatty acid requirements in pregnancy and lactation with special reference to brain development. Prog Lipid Res 20:31–40
Green P, Yavin E (1993) Elongation, desaturation, and esterification of essential fatty acids by fetal rat brain in vivo. J Lipid Res 34:2099–2107
Bayer SA, Altman J, Russo RJ, Zhang X (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83–144
Frederiksen K, McKay RD (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144–1151
Green P, Glozman S, Kamensky B, Yavin E (1999) Developmental changes in rat brain membrane lipids and fatty acids. The preferential prenatal accumulation of docosahexaenoic acid. J Lipid Res 40:960–966
Schiefermeier M, Yavin E (2002) n-3 Deficient and docosahexaenoic acid-enriched diets during critical periods of the developing prenatal rat brain. J Lipid Res 43:124–131
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
Amusquivar E, Schiffner S, Herrera E (2011) Evaluation of two methods for plasma fatty acid analysis by GC. Eur J Lipid Sci Technol 113:711–716
Sivan E, Homko CJ, Chen X, Reece EA, Boden G (1999) Effect of insulin on fat metabolism during and after normal pregnancy. Diabetes 48:834–838
Herrera EM, Knopp RH, Freinkel N (1969) Urinary excretion of epinephrine and norepinephrine during fasting in late pregnancy in the rat. Endocrinology 84:447–450
Raclot T, Groscolas R (1995) Selective mobilization of adipose tissue fatty acids during energy depletion in the rat. J Lipid Res 36:2164–2173
Raclot T, Mioskowski E, Bach AC, Groscolas R (1995) Selectivity of fatty acid mobilization: a general metabolic feature of adipose tissue. Am J Physiol 269:R1060-1067
Brenner RR (1974) The oxidative desaturation of unsaturated fatty acids in animals. Mol Cell Biochem 3:41–52
Cook HW (1991) Fatty acid desaturation and chain elongation in eucaryotes. In: Vance DE, Vance J (eds) Biochemistry of lipids, lipoproteins and membranes. Elsevier, Amsterdam, pp 141–169
Garg ML, Thomson AB, Clandinin MT (1990) Interactions of saturated, n-6 and n-3 polyunsaturated fatty acids to modulate arachidonic acid metabolism. J Lipid Res 31:271–277
Raz A, Kamin-Belsky N, Przedecki F, Obukowicz M (1998) Dietary fish oil inhibits delta6-desaturase activity. J Am Oil Chem Soc 75:241–245
Herrera E, Amusquivar E, Lopez-Soldado I, Ortega H (2006) Maternal lipid metabolism and placental lipid transfer. Horm Res 65(Suppl 3):59–64
Lorenzo M, Caldes T, Benito M, Medina JM (1981) Lipogenesis in vivo in maternal and foetal tissues during late gestation in the rat. Biochem J 198:425–428
Mercuri O, de Tomas ME, Itarte H (1979) Prenatal protein depletion and Delta9, Delta6 and Delta5 desaturases in the rat. Lipids 14:822–825
Campbell FM, Gordon MJ, Dutta-Roy AK (1996) Preferential uptake of long chain polyunsaturated fatty acids by isolated human placental membranes. Mol Cell Biochem 155:77–83
Ravel D, Chambaz J, Pepin D, Manier MC, Bereziat G (1985) Essential fatty acid interconversion during gestation in the rat. Biochim Biophys Acta 833:161–164
Chambaz J, Ravel D, Manier MC, Pepin D, Mulliez N, Bereziat G (1985) Essential fatty acids interconversion in the human fetal liver. Biol Neonate 47:136–140
Green P, Kamensky B, Yavin E (1997) Replenishment of docosahexaenoic acid in n-3 fatty acid-deficient fetal rats by intraamniotic ethyl-docosahexaenoate administration. J Neurosci Res 48:264–272
Amusquivar E, Ruperez FJ, Barbas C, Herrera E (2000) Low arachidonic acid rather than alpha-tocopherol is responsible for the delayed postnatal development in offspring of rats fed fish oil instead of olive oil during pregnancy and lactation. J Nutr 130:2855–2865
Acknowledgements
We thank Milagros Morante for her excellent technical assistance and pp-science-editing.com for editing and linguistic revision of the manuscript. This work was supported by grants from Universidad San Pablo-CEU (USP09-12), Fundación Ramón Areces of Spain (Grant CIVP16A1835), and the European Communities Commission, specific RTD program + Quality of Life and Management of Living Resources, PeriLip (QLK1-2001-00138). This work does not necessarily reflect the views of the Commission and in no way anticipates its future policy in this area.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Rights and permissions
About this article
Cite this article
López-Soldado, I., Ortega-Senovilla, H. & Herrera, E. Maternal adipose tissue becomes a source of fatty acids for the fetus in fasted pregnant rats given diets with different fatty acid compositions. Eur J Nutr 57, 2963–2974 (2018). https://doi.org/10.1007/s00394-017-1570-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-017-1570-4