Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Prepartum maternal diets supplemented with oilseeds alter the fatty acid profile in bovine neonatal plasma possibly through reduced placental expression of fatty acid transporter protein 4 and fatty acid translocase

Reza Salehi A and Divakar J. Ambrose A B C
+ Author Affiliations
- Author Affiliations

A Department of Agricultural, Food and Nutritional Science, 410 Agriculture/Forestry Centre, University of Alberta, Edmonton, AB T6G 2P5, Canada.

B Livestock Research Branch, Alberta Agriculture and Forestry, 7000 – 113 Street NW, Edmonton, AB T6H 5T6, Canada.

C Corresponding author. Email: divakar.ambrose@gov.ab.ca

Reproduction, Fertility and Development 29(9) 1846-1855 https://doi.org/10.1071/RD15476
Submitted: 14 November 2015  Accepted: 6 October 2016   Published: 12 December 2016

Abstract

In the present study, we determined the effects of maternal dietary fat and the type of fat on plasma fatty acids and the expression of placental fatty acid transporter genes. In Experiment 1, Holstein cows in the last 35 days of gestation received diets containing sunflower seed (n = 8; high in linoleic acid (LA)), canola seed (n = 7; high in oleic acid (OLA)) or no oilseed (n = 7; control). Fatty acids were quantified in dam and neonate plasma at calving. In Experiment 2, placental cotyledons were collected (LA: n = 4; OLA: n = 4; control: n = 5) to quantify gene expression. Maternal long-chain polyunsaturated fatty acids, neonatal total n-3 fatty acids and eicosapentaenoic acid (EPA) declined, whereas docosahexaenoic acid (DHA) and total fat tended to decline following fat supplementation prepartum. Feeding of LA versus OLA prepartum tended to increase peroxisome proliferator-activated receptor α (PPARA) expression, whereas peroxisome proliferator-activated receptor δ (PPARD) and peroxisome proliferator-activated receptor γ (PPARG) expression tended to be higher in OLA- than LA-fed cows. Expression of fatty acid transporter protein 4 (FATP4) and fatty acid translocase (FAT/CD36) expression was lower in placental tissue of cows fed fat compared with control cows. Reduced total n-3 fatty acids, EPA and DHA in neonates born of dams fed fat prepartum is likely due to changes in PPARs and reduced expression of placental FATP4 and FAT/CD36.

Additional keywords: canola, cotyledons, dairy cow, linoleic acid, oleic acid, placental transfer, PUFA, sunflower.


References

Ambrose, D. J., Kastelic, J. P., Corbett, R., Pitney, P. A., Petit, H. V., Small, J. A., and Zalkovic, P. (2006). Lower pregnancy losses in lactating dairy cows fed a diet enriched in alpha-linolenic acid. J. Dairy Sci. 89, 3066–3074.
Lower pregnancy losses in lactating dairy cows fed a diet enriched in alpha-linolenic acid.CrossRef | 1:CAS:528:DC%2BD28Xns1Cltb8%3D&md5=45b39c68c706bf2da5cae2590e9b4c09CAS |

Barak, Y., Nelson, M. C., Ong, E. S., Jones, Y. Z., Ruiz-Lozano, P., Chien, K. R., Koder, A., and Evans, R. M. (1999). PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol. Cell 4, 585–595.
PPAR gamma is required for placental, cardiac, and adipose tissue development.CrossRef | 1:CAS:528:DyaK1MXntFCgsLY%3D&md5=55861adbfbe2b0993d433e0889e2b830CAS |

Battaglia, F. C., and Meschia, G. (1988). Fetal nutrition. Annu. Rev. Nutr. 8, 43–61.
Fetal nutrition.CrossRef | 1:CAS:528:DyaL1cXlvV2isbc%3D&md5=6fdf98edaa9ce223fafcfa77be3f76f7CAS |

Blank, C., Neumann, M. A., Makrides, M., and Gibson, R. A. (2002). Optimizing DHA levels in piglets by lowering the linoleic acid to alpha-linolenic acid ratio. J. Lipid Res. 43, 1537–1543.
Optimizing DHA levels in piglets by lowering the linoleic acid to alpha-linolenic acid ratio.CrossRef | 1:CAS:528:DC%2BD38XnsFKhtbo%3D&md5=08b71d856523dce2d634dcf916ace545CAS |

Cabrero, A., Alegret, M., Sanchez, R. M., Adzet, T., Laguna, J. C., and Vazquez, M. (2001). Bezafibrate reduces mRNA levels of adipocyte markers and increases fatty acid oxidation in primary culture of adipocytes. Diabetes 50, 1883–1890.
Bezafibrate reduces mRNA levels of adipocyte markers and increases fatty acid oxidation in primary culture of adipocytes.CrossRef | 1:CAS:528:DC%2BD3MXlslKmsrs%3D&md5=04df74969bdc48c13d8a4e3c9803b901CAS |

Calder, P. C., and Grimble, R. F. (2002). Polyunsaturated fatty acids, inflammation and immunity. Eur. J. Clin. Nutr. 56, S14–S19.
Polyunsaturated fatty acids, inflammation and immunity.CrossRef | 1:CAS:528:DC%2BD38Xmt1Wnsrw%3D&md5=45fd598f5488d2bce899d8f694d47774CAS |

Campbell, F. M., Gordon, M. J., and Dutta-Roy, A. K. (1994). Plasma membrane fatty acid-binding protein (FABPpm) of the sheep placenta. Biochim. Biophys. Acta 1214, 187–192.
Plasma membrane fatty acid-binding protein (FABPpm) of the sheep placenta.CrossRef | 1:CAS:528:DyaK2cXmt1Cmsbo%3D&md5=8c4d659cc5792fa23d82334d9e1a28cfCAS |

Campbell, F. M., Clohessy, A. M., Gordon, M. J., Page, K. R., and Dutta-Roy, A. K. (1997). Uptake of long chain fatty acids by human placental choriocarcinoma (BeWo) cells: role of plasma membrane fatty acid-binding protein. J. Lipid Res. 38, 2558–2568.
| 1:CAS:528:DyaK1cXitVyjsQ%3D%3D&md5=e265aa508917fc1cc8af8d15c42d7cc5CAS |

Campbell, F. M., Bush, P. G., Veerkamp, J. H., and Dutta-Roy, A. K. (1998a). Detection and cellular localization of plasma membrane-associated and cytoplasmic fatty acid-binding proteins in human placenta. Placenta 19, 409–415.
Detection and cellular localization of plasma membrane-associated and cytoplasmic fatty acid-binding proteins in human placenta.CrossRef | 1:CAS:528:DyaK1cXlt1agtrc%3D&md5=9f0058a1ccdc88fd2c1e54934c8801aeCAS |

Campbell, F. M., Gordon, M. J., and Dutta-Roy, A. K. (1998b). Placental membrane fatty acid-binding protein preferentially binds arachidonic and docosahexaenoic acids. Life Sci. 63, 235–240.
Placental membrane fatty acid-binding protein preferentially binds arachidonic and docosahexaenoic acids.CrossRef | 1:CAS:528:DyaK1cXktFOgt7g%3D&md5=4caedcc83a536814f144aa50e8fae1b5CAS |

Chambaz, J., Ravel, D., Manier, M. C., Pepin, D., Mulliez, N., and Bereziat, G. (1985). Essential fatty acids interconversion in the human fetal liver. Biol. Neonate 47, 136–140.
Essential fatty acids interconversion in the human fetal liver.CrossRef | 1:CAS:528:DyaL2MXhtlSqsL0%3D&md5=d7a7004e857b5d9dbc8391c861781f87CAS |

Cho, K. J., Moon, H. E., Moini, H., Packer, L., Yoon, D. Y., and Chung, A. S. (2003). Alpha-lipoic acid inhibits adipocyte differentiation by regulating pro-adipogenic transcription factors via mitogen-activated protein kinase pathways. J. Biol. Chem. 278, 34 823–34 833.
Alpha-lipoic acid inhibits adipocyte differentiation by regulating pro-adipogenic transcription factors via mitogen-activated protein kinase pathways.CrossRef | 1:CAS:528:DC%2BD3sXntVWqsLk%3D&md5=3a7d0bcd296009ea7eb2159ae1963678CAS |

Connor, W. E., and Neuringer, M. (1988). The effects of n-3 fatty acid deficiency and repletion upon the fatty acid composition and function of the brain and retina. Prog. Clin. Biol. Res. 282, 275–294.
| 1:CAS:528:DyaL1MXhvFWmu7k%3D&md5=bfc51601e7e84320f2c6c96dd9949fd8CAS |

Cruz-Hernandez, C., Kramer, J. K., Kennelly, J. J., Glimm, D. R., Sorensen, B. M., Okine, E. K., Goonewardene, L. A., and Weselake, R. J. (2007). Evaluating the conjugated linoleic acid and trans 18:1 isomers in milk fat of dairy cows fed increasing amounts of sunflower oil and a constant level of fish oil. J. Dairy Sci. 90, 3786–3801.
Evaluating the conjugated linoleic acid and trans 18:1 isomers in milk fat of dairy cows fed increasing amounts of sunflower oil and a constant level of fish oil.CrossRef | 1:CAS:528:DC%2BD2sXot1Oltb0%3D&md5=b4194f8b9a0aac3d091d6f8290bfc88eCAS |

Daoud, G., Simoneau, L., Masse, A., Rassart, E., and Lafond, J. (2005). Expression of cFABP and PPAR in trophoblast cells: effect of PPAR ligands on linoleic acid uptake and differentiation. Biochim. Biophys. Acta 1687, 181–194.
Expression of cFABP and PPAR in trophoblast cells: effect of PPAR ligands on linoleic acid uptake and differentiation.CrossRef | 1:CAS:528:DC%2BD2MXhtlSrsLs%3D&md5=0ffc907aea999879a93697b164a6a17dCAS |

Duttaroy, A. K. (2000). Transport mechanisms for long-chain polyunsaturated fatty acids in the human placenta. Am. J. Clin. Nutr. 71, 315S–322S.
| 1:CAS:528:DC%2BD3cXlsFKjtA%3D%3D&md5=d01bca6b4c471198ee72bb8ee03c331fCAS |

Duttaroy, A. K. (2004). Fetal growth and development: roles of fatty acid transport proteins and nuclear transcription factors in human placenta. Indian J. Exp. Biol. 42, 747–757.
| 1:CAS:528:DC%2BD2cXhtVakt7zJ&md5=08a88b7592756da53b61ea6a37c1439dCAS |

Elias, S. L., and Innis, S. M. (2001). Infant plasma trans, n-6, and n-3 fatty acids and conjugated linoleic acids are related to maternal plasma fatty acids, length of gestation, and birth weight and length. Am. J. Clin. Nutr. 73, 807–814.
| 1:CAS:528:DC%2BD3MXisFWhs7g%3D&md5=13855c29eec748ee86a603147350e5c5CAS |

Elphick, M. C., Hull, D., and Broughton Pipkin, F. (1979). The transfer of fatty acids across the sheep placenta. J. Dev. Physiol. 1, 31–45.
| 1:CAS:528:DyaE1MXkvVymsLY%3D&md5=f9c81e2f1b732424b4a9f97e372f5794CAS |

Folch, J., Lees, M., and Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497–509.
| 1:STN:280:DyaG2s%2FnsFCjtw%3D%3D&md5=b92f7b65bbb4bd15d7ee84c7307ff606CAS |

Friesen, R. W., and Innis, S. M. (2010). Linoleic acid is associated with lower long-chain n-6 and n-3 fatty acids in red blood cell lipids of Canadian pregnant women. Am. J. Clin. Nutr. 91, 23–31.
Linoleic acid is associated with lower long-chain n-6 and n-3 fatty acids in red blood cell lipids of Canadian pregnant women.CrossRef | 1:CAS:528:DC%2BD1MXhs1WlsbjJ&md5=26b280a07ee15c770c03d4850319ccfcCAS |

Garcia, M., Greco, L. F., Favoreto, M. G., Marsola, R. S., Martins, L. T., Bisinotto, R. S., Shin, J. H., Lock, A. L., Block, E., Thatcher, W. W., Santos, J. E., and Staples, C. R. (2014a). Effect of supplementing fat to pregnant nonlactating cows on colostral fatty acid profile and passive immunity of the newborn calf. J. Dairy Sci. 97, 392–405.
Effect of supplementing fat to pregnant nonlactating cows on colostral fatty acid profile and passive immunity of the newborn calf.CrossRef | 1:CAS:528:DC%2BC3sXhslOlsL7J&md5=8b004f2b9255d8d5623554f27ee95c8dCAS |

Garcia, M., Greco, L. F., Favoreto, M. G., Marsola, R. S., Wang, D., Shin, J. H., Block, E., Thatcher, W. W., Santos, J. E., and Staples, C. R. (2014b). Effect of supplementing essential fatty acids to pregnant nonlactating Holstein cows and their preweaned calves on calf performance, immune response, and health. J. Dairy Sci. 97, 5045–5064.
Effect of supplementing essential fatty acids to pregnant nonlactating Holstein cows and their preweaned calves on calf performance, immune response, and health.CrossRef | 1:CAS:528:DC%2BC2cXpvFWmtr0%3D&md5=dadf9b721a7aa1d59211411ee5daed5aCAS |

Hamilton, J. A. (1998). Fatty acid transport: difficult or easy? J. Lipid Res. 39, 467–481.
| 1:CAS:528:DyaK1cXit1Kmsbk%3D&md5=8f53c7196623494873a9dd95e4e6920bCAS |

Hamilton, J. A., and Kamp, F. (1999). How are free fatty acids transported in membranes? Is it by proteins or by free diffusion through the lipids? Diabetes 48, 2255–2269.
How are free fatty acids transported in membranes? Is it by proteins or by free diffusion through the lipids?CrossRef | 1:CAS:528:DyaK1MXnslOqtr0%3D&md5=f209a1d7a42748059f7ddd1b04f81cafCAS |

Harnack, K., Andersen, G., and Somoza, V. (2009). Quantitation of alpha-linolenic acid elongation to eicosapentaenoic and docosahexaenoic acid as affected by the ratio of n6/n3 fatty acids. Nutr. Metab. (Lond) 6, 8.
Quantitation of alpha-linolenic acid elongation to eicosapentaenoic and docosahexaenoic acid as affected by the ratio of n6/n3 fatty acids.CrossRef |

Hull, D., and Stammers, J. P. (1985). Placental transfer of fatty acids. Biochem. Soc. Trans. 13, 821–822.
Placental transfer of fatty acids.CrossRef | 1:CAS:528:DyaL2MXltVamt7s%3D&md5=66993de3043aae7c7c341f4b39c6464cCAS |

Kuhn, D. C., and Crawford, M. (1986). Placental essential fatty acid transport and prostaglandin synthesis. Prog. Lipid Res. 25, 345–353.
Placental essential fatty acid transport and prostaglandin synthesis.CrossRef | 1:CAS:528:DyaL2sXhtlahurg%3D&md5=e7b22f277dc39de3324a73e5f89e40bdCAS |

Kuhn, D. C., Crawford, M. A., Gordon, G. B., and Stuart, M. J. (1988). Aspects of in vitro placental perfusion: effects of hyperoxia and phenol red. Placenta 9, 201–213.
Aspects of in vitro placental perfusion: effects of hyperoxia and phenol red.CrossRef | 1:STN:280:DyaL1c3ovFKjtg%3D%3D&md5=ece7b8f2a6cc2dce7793492001e473eeCAS |

Laarman, A. H., Ruiz-Sanchez, A. L., Sugino, T., Guan, L. L., and Oba, M. (2012). Effects of feeding a calf starter on molecular adaptations in the ruminal epithelium and liver of Holstein dairy calves. J. Dairy Sci. 95, 2585–2594.
Effects of feeding a calf starter on molecular adaptations in the ruminal epithelium and liver of Holstein dairy calves.CrossRef | 1:CAS:528:DC%2BC38XlvFyhtLY%3D&md5=3b035f191c75dd77ea077e000cd5042dCAS |

Larqué, E., Krauss-Etschmann, S., Campoy, C., Hartl, D., Linde, J., Klingler, M., Demmelmair, H., Caño, A., Gil, A., Bondy, B., and Koletzko, B. (2006). Docosahexaenoic acid supply in pregnancy affects placental expression of fatty acid transport proteins. Am. J. Clin. Nutr. 84, 853–861.

Leat, W. M., and Harrison, F. A. (1980). Transfer of long-chain fatty acids to the fetal and neonatal lamb. J. Dev. Physiol. 2, 257–274.
| 1:CAS:528:DyaL3MXhsFCjtL0%3D&md5=f106a39841eb91eb5e549e977b300ae1CAS |

Martínez, N., Capobianco, E., White, V., Pustovrh, M. C., Higa, R., and Jawerbaum, A. (2008). Peroxisome proliferator-activated receptor alpha activation regulates lipid metabolism in the feto-placental unit from diabetic rats. Reproduction 136, 95–103.
Peroxisome proliferator-activated receptor alpha activation regulates lipid metabolism in the feto-placental unit from diabetic rats.CrossRef |

Moallem, U., and Zachut, M. (2012). Short communication: the effects of supplementation of various n-3 fatty acids to late-pregnant dairy cows on plasma fatty acid composition of the newborn calves. J. Dairy Sci. 95, 4055–4058.
Short communication: the effects of supplementation of various n-3 fatty acids to late-pregnant dairy cows on plasma fatty acid composition of the newborn calves.CrossRef | 1:CAS:528:DC%2BC38XoslGrt70%3D&md5=112406c3ba5b369f2244924823beb44eCAS |

Neuringer, M., Connor, W. E., Lin, D. S., Barstad, L., and 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.
Biochemical and functional effects of prenatal and postnatal omega 3 fatty acid deficiency on retina and brain in rhesus monkeys.CrossRef | 1:CAS:528:DyaL28XksVWks7o%3D&md5=a0013c2eaa3c607222ad615dd1982ba4CAS |

Novak, E. M., King, D. J., and Innis, S. M. (2012). Low linoleic acid may facilitate Delta6 desaturase activity and docosahexaenoic acid accretion in human fetal development. Prostaglandins Leukot. Essent. Fatty Acids 86, 93–98.
Low linoleic acid may facilitate Delta6 desaturase activity and docosahexaenoic acid accretion in human fetal development.CrossRef | 1:CAS:528:DC%2BC38XjtVWmu7g%3D&md5=3b04af69f80e0ce55ee25402eb366cb9CAS |

Olfert, D. E., Cross, B. M., and McWilliam, A. A. (Eds) (1993). ‘Guide to the Care and Use of Experimental Animals. 2nd ed. Vol. 1.’ (Canadian Council on Animal Care: Ottawa, Canada.)

Rump, P., Mensink, R. P., Kester, A. D., and Hornstra, G. (2001). Essential fatty acid composition of plasma phospholipids and birth weight: a study in term neonates. Am. J. Clin. Nutr. 73, 797–806.
| 1:CAS:528:DC%2BD3MXisFWhs7s%3D&md5=78c417501e26d26d7eea6ed6a9735cbaCAS |

Salehi, R., Colazo, M. G., Oba, M., and Ambrose, D. J. (2016). Effects of prepartum diets supplemented with rolled oilseeds on calf birth weight, postpartum health, feed intake, milk yield, and reproductive performance of dairy cows. J. Dairy Sci. 99, 3584–3597.
Effects of prepartum diets supplemented with rolled oilseeds on calf birth weight, postpartum health, feed intake, milk yield, and reproductive performance of dairy cows.CrossRef | 1:CAS:528:DC%2BC28XktVOnu7w%3D&md5=a5eaae9d7f4b62919f17b374a5ab7881CAS |

Salehi, R., Ambrose, D. J., and Oba, M. (2016a). Short communication: effects of prepartum diets supplemented with rolled oilseeds on Brix values and fatty acid profile of colostrum. J. Dairy Sci. 99, 3598–3601.
Short communication: effects of prepartum diets supplemented with rolled oilseeds on Brix values and fatty acid profile of colostrum.CrossRef | 1:CAS:528:DC%2BC28XktVOntLc%3D&md5=a929ca3deea438612394ffab8586e9d3CAS |

Schlau, N., Guan, L. L., and Oba, M. (2012). The relationship between rumen acidosis resistance and expression of genes involved in regulation of intracellular pH and butyrate metabolism of ruminal epithelial cells in steers. J. Dairy Sci. 95, 5866–5875.
The relationship between rumen acidosis resistance and expression of genes involved in regulation of intracellular pH and butyrate metabolism of ruminal epithelial cells in steers.CrossRef | 1:CAS:528:DC%2BC38XhsVCns7vK&md5=d6ae48f5bc316ed6d760a1e86a9ac823CAS |

Schroit, A. J., and Gallily, R. (1979). Macrophage fatty acid composition and phagocytosis: effect of unsaturation on cellular phagocytic activity. Immunology 36, 199–205.
| 1:CAS:528:DyaE1MXksFegsLw%3D&md5=dc4a9d8d7c9e02cb9469c9092402d72aCAS |

Shand, J. H., and Noble, R. C. (1981). The metabolism of 18:0 and 18:2(n-6) by the ovine placenta at 120 and 150 days of gestation. Lipids 16, 68–71.
The metabolism of 18:0 and 18:2(n-6) by the ovine placenta at 120 and 150 days of gestation.CrossRef | 1:CAS:528:DyaL3MXhtFylu7o%3D&md5=1f4557f869c267f86edf4a022586bd9bCAS |

Silvestre, F. T., Carvalho, T. S., Francisco, N., Santos, J. E., Staples, C. R., Jenkins, T. C., and Thatcher, W. W. (2011). Effects of differential supplementation of fatty acids during the peripartum and breeding periods of Holstein cows: I. Uterine and metabolic responses, reproduction, and lactation. J. Dairy Sci. 94, 189–204.
Effects of differential supplementation of fatty acids during the peripartum and breeding periods of Holstein cows: I. Uterine and metabolic responses, reproduction, and lactation.CrossRef | 1:CAS:528:DC%2BC3MXjslCnt78%3D&md5=37ae3a708596b61d2ceaf754b990b8f2CAS |

Szitanyi, P., Koletzko, B., Mydlilova, A., and Demmelmair, H. (1999). Metabolism of 13C-labeled linoleic acid in newborn infants during the first week of life. Pediatr. Res. 45, 669–673.
Metabolism of 13C-labeled linoleic acid in newborn infants during the first week of life.CrossRef | 1:CAS:528:DyaK1MXjtFCrtrk%3D&md5=4ffefa9b1922db3ce23b7382a83e085fCAS |

Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.1.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.CrossRef |

Wang, Y. X., Lee, C. H., Tiep, S., Yu, R. T., Ham, J., Kang, H., and Evans, R. M. (2003). Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 113, 159–170.
Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity.CrossRef | 1:CAS:528:DC%2BD3sXjtlOqs7k%3D&md5=c8566ec80bdb609f1ac473a0d665cc36CAS |

Weisinger, H. S., Armitage, J. A., Sinclair, A. J., Vingrys, A. J., Burns, P. L., and Weisinger, R. S. (2001). Perinatal omega-3 fatty acid deficiency affects blood pressure later in life. Nat. Med. 7, 258–259.
Perinatal omega-3 fatty acid deficiency affects blood pressure later in life.CrossRef | 1:CAS:528:DC%2BD3MXhvVOltb0%3D&md5=976edf45f0bdf09acc7531482c5a6cd1CAS |



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