Challenges in enriching milk fat with polyunsaturated fatty acids

Journal of Animal Science and Biotechnology

Benjamin A. Corl²  Jennifer Stamey Lanier¹ 

[1] Phibro Animal Health Corporation, Teaneck, NJ, USA;Department of Dairy Science, Virginia Tech, Blacksburg 24061-0315, VA, USA

关键词: Polyunsaturated fatty acids;    Milk fat;    Dairy cow;   

Others  :  1217375
DOI  :  10.1186/s40104-015-0025-0

 received in 2015-01-27, accepted in 2015-06-02,  发布年份 2015

【 摘 要 】

Milk fatty acid composition is determined by several factors including diet. The milk fatty acid profile of dairy cows is low in polyunsaturated fatty acids, especially those of the n-3 series. Efforts to change and influence fatty acid profile with longer chain polyunsaturated fatty acids have proven challenging. Several barriers prevent easy transfer of dietary polyunsaturated fatty acids to milk fat including rumen biohydrogenation and fatty acid esterification. The potential for cellular uptake and differences in fatty acid incorporation into milk fat might also have an effect, though this has received less research effort. Given physiological impediments to enriching milk fat with polyunsaturated fatty acids, manipulating the genome of the cow might provide a greater increase than diet alone, but this too may be challenged by the physiology of the cow.

【 授权许可】

   
2015 Lanier and Corl.

【 图 表 】

Fig. 1.

【 参考文献 】

• [1]Jenkins TC, McGuire MA: Major advances in nutrition: Impact on milk composition. J Dairy Sci 2006, 89(4):1302-10.
• [2]Kelm SC, Freeman AE: Direct and correlated responses to selection for milk yield: results and conclusions of regional project NC-2, "improvement of dairy cattle through breeding, with emphasis on selection". NC-2 Technical Committee. J Dairy Sci 2000, 83(12):2721-32.
• [3]Kay JK, Weber WJ, Moore CE, Bauman DE, Hansen LB, Chester-Jones H, et al.: Effects of week of lactation and genetic selection for milk yield on milk fatty acid composition in Holstein cows. J Dairy Sci 2005, 88(11):3886-93.
• [4]Lock AL, Bauman DE: Modifying milk fat composition of dairy cows to enhance fatty acids beneficial to human health. Lipids 2004, 39(12):1197-206.
• [5]Naik PK: Bypass fat in dairy ration - a review. Anim Nutr Feed Technol 2013, 13(1):147-63.
• [6]Broun P, Gettner S, Somerville C: Genetic engineering of plant lipids. Annu Rev Nutr 1999, 19:197-216.
• [7]Hazebroek JP: Analysis of genetically modified oils. Prog Lipid Res 2000, 39(6):477-506.
• [8]Drackley JK: Interorgan lipid and fatty acid metabolism in growing ruminants. In Biology of Metabolism in Growing Animals. Biology of Growing Animals. Edited by Burrin DG, Mersmann HJ. Elsevier Ltd, New York; 2005:323-50.
• [9]Loor JJ, Ueda K, Ferlay A, Chilliard Y, Doreau M: Biohydrogenation, duodenal flow, and intestinal digestibility of trans fatty acids and conjugated linoleic acids in response to dietary forage:concentrate ratio and linseed oil in dairy cows. J Dairy Sci 2004, 87(8):2472-85.
• [10]Kalscheur KF, Teter BB, Piperova LS, Erdman RA: Effect of fat source on duodenal flow of trans-C18:1 fatty acids and milk fat production in dairy cows. J Dairy Sci 1997, 80(9):2115-26.
• [11]Kalscheur KF, Teter BB, Piperova LS, Erdman RA: Effect of dietary forage concentration and buffer addition on duodenal flow of trans-C18:1 fatty acids and milk fat production in dairy cows. J Dairy Sci 1997, 80(9):2104-14.
• [12]Dawson RM, Hemington N, Hazlewood GP: On the role of higher plant and microbial lipases in the ruminal hydrolysis of grass lipids. Br J Nutr 1977, 38(2):225-32.
• [13]Hawke JC, Silcock WR: Lipolysis and hydrogenation in the rumen. Biochem J 1969, 112(1):131-2.
• [14]Kepler CR, Tucker WP, Tove SB: Biohydrogenation of unsaturated fatty acids. IV. Substrate specificity and inhibition of linoleate delta-12-cis, delta-11-trans-isomerase from Butyrivibrio fibrisolvens. J Biol Chem 1970, 245(14):3612-20.
• [15]Van Nevel CJ, Demeyer DI: Influence of pH on lipolysis and biohydrogenation of soybean oil by rumen contents in vitro. Reprod Nutr Dev 1996, 36(1):53-63.
• [16]Hazlewood GP, Kemp P, Lander D, Dawson RMC: C-18 unsaturated fatty acid hydrogenation patterns of some rumen bacteria and their ability to hydrolyze exogenous phospholipid. Br J Nutr 1976, 35(2):293-7.
• [17]Singh S, Hawke JC: The in vitro lipolysis and biohydrogenation of monogalactosyldiglyceride by whole rumen contents and its fractions. J Sci Food Agric 1979, 30(6):603-12.
• [18]Harfoot CG, Hazlewood GP: Lipid metabolism in the rumen. In The Rumen Microbial Ecosystem. Edited by Hobson PN. Elsevier Applied Science Publishers, London; 1988:285-322.
• [19]Polan CE, Mc Neill JJ, Tove SB: Biohydrogenation of unsaturated fatty acids by rumen bacteria. J Bacteriol 1964, 88(4):1056-64.
• [20]Kemp P, Lander DJ: Hydrogenation in vitro of α-linolenic acid to stearic acid by mixed cultures of pure strains of rumen bacteria. J Gen Micro 1984, 130(MAR):527-33.
• [21]Lourenco M, Ramos-Morales E, Wallace RJ: The role of microbes in rumen lipolysis and biohydrogenation and their manipulation. Animal 2010, 4(7):1008-23.
• [22]Yokoyama MT, Davis CL: Hydrogenation of unsaturated fatty acids by Treponema (Borrelia) strain B 2 5, a rumen spirochete. J Bacteriol 1971, 107(2):519-27.
• [23]Kepler CR, Tove SB: Biohydrogenation of unsaturated fatty acids. 3. Purification and properties of a linoleate delta-12-cis, delta-11-trans-isomerase from Butyrivibrio fibrisolvens. J Biol Chem 1967, 242(24):5686-92.
• [24]Davis C, Brown R, editors. Low-fat milk syndrome. Physiology of digestion and metabolism in the ruminant. Proceedings of the third international symposium, Cambridge, England; August 1969.; 1970: Newcastle-upon-Tyne: Oriel Press.
• [25]Griinari JM, Dwyer DA, McGuire MA, Bauman DE, Palmquist DL, Nurmela KV: Trans-octadecenoic acids and milk fat depression in lactating dairy cows. J Dairy Sci 1998, 81(5):1251-61.
• [26]Bauman DE, Griinari JM: Nutritional regulation of milk fat synthesis. Annu Rev Nutr 2003, 23:203-27.
• [27]Jenkins TC, Wallace RJ, Moate PJ, Mosley EE: Board-invited review: recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J Anim Sci 2008, 86(2):397-412.
• [28]Baumgard LH, Corl BA, Dwyer DA, Saebo A, Bauman DE: Identification of the conjugated linoleic acid isomer that inhibits milk fat synthesis. Am J Physiol Regul Integr Comp Physiol 2000, 278(1):R179-84.
• [29]Peterson DG, Baumgard LH, Bauman DE: Short communication: milk fat response to low doses of tran-10, cis-12 conjugated linoleic acid (CLA). J Dairy Sci 2002, 85(7):1764-6.
• [30]Lock AL, Tyburczy C, Dwyer DA, Harvatine KJ, Destaillats F, Mouloungui Z, et al.: Trans-10 octadecenoic acid does not reduce milk fat synthesis in dairy cows. J Nutr 2007, 137(1):71-6.
• [31]Klein CM, Jenkins TC: Docosahexaenoic acid elevates trans-18:1 isomers but is not directly converted into trans-18:1 isomers in ruminal batch cultures. J Dairy Sci 2011, 94(9):4676-83.
• [32]AbuGhazaleh AA, Jenkins TC: Short communication: docosahexaenoic acid promotes vaccenic acid accumulation in mixed ruminal cultures when incubated with linoleic acid. J Dairy Sci 2004, 87(4):1047-50.
• [33]Whitlock LA, Schingoethe DJ, AbuGhazaleh AA, Hippen AR, Kalscheur KF: Milk production and composition from cows fed small amounts of fish oil with extruded soybeans. J Dairy Sci 2006, 89(10):3972-80.
• [34]Whitlock LA, Schingoethe DJ, Hippen AR, Kalscheur KF, Baer RJ, Ramaswamy N, et al.: Fish oil and extruded soybeans fed in combination increase conjugated linoleic acids in milk of dairy cows more than when fed separately. J Dairy Sci 2002, 85(1):234-43.
• [35]Santos JE, Bilby TR, Thatcher WW, Staples CR, Silvestre FT: Long chain fatty acids of diet as factors influencing reproduction in cattle. Reprod Domest Anim 2008, 43(Suppl 2):23-30.
• [36]Mattos R, Staples CR, Arteche A, Wiltbank MC, Diaz FJ, Jenkins TC, et al.: The effects of feeding fish oil on uterine secretion of PGF2alpha, milk composition, and metabolic status of periparturient Holstein cows. J Dairy Sci 2004, 87(4):921-32.
• [37]Mattos R, Staples CR, Thatcher WW: Effects of dietary fatty acids on reproduction in ruminants. Rev Reprod 2000, 5(1):38-45.
• [38]Staples CR, Burke JM, Thatcher WW: Influence of supplemental fats on reproductive tissues and performance of lactating cows. J Dairy Sci 1998, 81(3):856-71.
• [39]Jenkins TC, Bridges WC: Protection of fatty acids against ruminal biohydrogenation in cattle. Eur J Lipid Sci Tech 2007, 109(8):778-89.
• [40]Castaneda-Gutierrez E, de Veth MJ, Lock AL, Dwyer DA, Murphy KD, Bauman DE: Effect of supplementation with calcium salts of fish oil on n-3 fatty acids in milk fat. J Dairy Sci 2007, 90(9):4149-56.
• [41]Perfield JW 2nd, Lock AL, Pfeiffer AM, Bauman DE: Effects of amide-protected and lipid-encapsulated conjugated linoleic acid supplements on milk fat synthesis. J Dairy Sci 2004, 87(9):3010-6.
• [42]Stamey JA, Shepherd DM, de Veth MJ, Corl BA: Use of algae or algal oil rich in n-3 fatty acids as a feed supplement for dairy cattle. J Dairy Sci 2012, 95(9):5269-75.
• [43]Noble RC: Digestion, absorption and transport of lipids in ruminant animals. Prog Lipid Res 1978, 17(1):55-91.
• [44]Bauchart D: Lipid absorption and transport in ruminants. J Dairy Sci 1993, 76(12):3864-81.
• [45]Jenkins TC: Lipid metabolism in the rumen. J Dairy Sci 1993, 76(12):3851-63.
• [46]Palmquist DL: A kinetic concepto of lipid transport in ruminants. J Dairy Sci 1976, 59(3):355-63.
• [47]Palmquist DL, Mattos W: Turnover of lipoproteins and transfer to milk fat of dietary (1-Carbon-14) linoleic acid in lactating cows. J Dairy Sci 1978, 61(5):561-5.
• [48]Emery RS: Deposition, secretion, transport and oxidation of fat in ruminants. J Anim Sci 1979, 48(6):1530-7.
• [49]Raphael BC, Dimick PS, Puppione DL: Lipid characterization of bovine serum lipoproteins throughout gestation and lactation. J Dairy Sci 1973, 56(8):1025-32.
• [50]Litherland NB, Thire S, Beaulieu AD, Reynolds CK, Benson JA, Drackley JK: Dry matter intake is decreased more by abomasal infusion of unsaturated free fatty acids than by unsaturated triglycerides. J Dairy Sci 2005, 88(2):632-43.
• [51]Drackley JK: ADSA Foundation Scholar Award. Biology of dairy cows during the transition period: the final frontier? J Dairy Sci 1999, 82(11):2259-73.
• [52]Harvatine KJ, Bauman DE: Characterization of the acute lactational response to trans-10, cis-12 conjugated linoleic acid. J Dairy Sci 2011, 94(12):6047-56.
• [53]Brumby PE, Storry JE, Sutton JD: Metabolism of cod-liver oil in relation to milk fat secretion. J Dairy Res 1972, 39(1):167-82.
• [54]Kitessa SM, Gulati SK, Ashes JR, Fleck E, Scott TW, Nichols PD: Utilisation of fish oil in ruminants - I. Fish oil metabolism in sheep. Anim Feed Sci Tech 2001, 89(3–4):189-99.
• [55]Offer NW, Speake BK, Dixon J, Marsden M: Effect of fish-oil supplementation on levels of (n-3) poly-unsaturated fatty acids in the lipoprotein fractions of bovine plasma. Animal Science 2001, 73:523-31.
• [56]Christie WW, Noble RC, Clegg RA: The hydrolysis of very low density lipoproteins and chylomicrons of intestinal origin by lipoprotein lipase in ruminants. Lipids 1986, 21(3):252-3.
• [57]Moore JH, Christie WW: Lipid metabolism in the mammary gland of ruminant animals. Prog Lipid Res 1979, 17(4):347-95.
• [58]Mansbridge RJ, Blake JS: Nutritional factors affecting the fatty acid composition of bovine milk. Br J Nutr 1997, 78(Suppl 1):S37-47.
• [59]Mosley EE, Shafii Dagger B, Moate PJ, McGuire MA: cis-9, trans-11 conjugated linoleic acid is synthesized directly from vaccenic acid in lactating dairy cattle. J Nutr 2006, 136(3):570-5.
• [60]Loor JJ, Quinlan LE, Bandara ABPA, Herbein JH: Distribution of trans-vaccenic acid and cis9,trans11-conjugated linoleic acid (rumenic acid) in blood plasma lipid fractions and secretion in milk fat of Jersey cows fed canola or soybean oil. Animal Research 2002, 51(2):119-34.
• [61]Nielsen MO, Jakobsen K: Changes in mammary uptake of free fatty acids, triglyceride, cholesterol and phospholipid in relation to milk synthesis during lactation in goats. Comp Biochem Physiol A Physiol 1994, 109(4):857-67.
• [62]Qi K, Seo T, Al-Haideri M, Worgall TS, Vogel T, Carpentier YA, et al.: Omega-3 triglycerides modify blood clearance and tissue targeting pathways of lipid emulsions. Biochemistry 2002, 41(9):3119-27.
• [63]Qi K, Seo T, Jiang Z, Carpentier YA, Deckelbaum RJ: Triglycerides in fish oil affect the blood clearance of lipid emulsions containing long- and medium-chain triglycerides in mice. J Nutr 2006, 136(11):2766-72.
• [64]Murray-Taylor FM, Ho YY, Densupsoontorn N, Chang CL, Deckelbaum RJ, Seo T: n-3, but not n-6 lipid particle uptake requires cell surface anchoring. Biochem Biophys Res Commun 2010, 392(2):135-9.
• [65]Park Y, Jones PG, Harris WS: Triacylglycerol-rich lipoprotein margination: a potential surrogate for whole-body lipoprotein lipase activity and effects of eicosapentaenoic and docosahexaenoic acids. Am J Clin Nutr 2004, 80(1):45-50.
• [66]Bionaz M, Loor JJ: Gene networks driving bovine milk fat synthesis during the lactation cycle. Bmc Genomics 2008, 9:366. BioMed Central Full Text
• [67]Pohl J, Ring A, Korkmaz U, Ehehalt R, Stremmel W: FAT/CD36-mediated long-chain fatty acid uptake in adipocytes requires plasma membrane rafts. Mol Biol Cell 2005, 16(1):24-31.
• [68]Chapkin RS, McMurray DN, Davidson LA, Patil BS, Fan YY, Lupton JR: Bioactive dietary long-chain fatty acids: emerging mechanisms of action. Br J Nutr 2008, 100(6):1152-7.
• [69]McArthur MJ, Atshaves BP, Frolov A, Foxworth WD, Kier AB, Schroeder F: Cellular uptake and intracellular trafficking of long chain fatty acids. J Lipid Res 1999, 40(8):1371-83.
• [70]Sandoval A, Fraisl P, Arias-Barrau E, Dirusso CC, Singer D, Sealls W, et al.: Fatty acid transport and activation and the expression patterns of genes involved in fatty acid trafficking. Arch Biochem Biophys 2008, 477(2):363-71.
• [71]Storch J, Corsico B: The emerging functions and mechanisms of mammalian fatty acid-binding proteins. Annu Rev Nutr 2008, 28:73-95.
• [72]Mather IH: A review and proposed nomenclature for major proteins of the milk-fat globule membrane. J Dairy Sci 2000, 83(2):203-47.
• [73]Specht B, Bartetzko N, Hohoff C, Kuhl H, Franke R, Borchers T, et al.: Mammary derived growth inhibitor is not a distinct protein but a mix of heart-type and adipocyte-type fatty acid-binding protein. J Biol Chem 1996, 271(33):19943-9.
• [74]Spener F, Unterberg C, Borchers T, Grosse R: Characteristics of fatty acid-binding proteins and their relation to mammary-derived growth inhibitor. Mol Cell Biochem 1990, 98(1–2):57-68.
• [75]Yang Y, Spitzer E, Kenney N, Zschiesche W, Li M, Kromminga A, et al.: Members of the fatty acid binding protein family are differentiation factors for the mammary gland. J Cell Biol 1994, 127(4):1097-109.
• [76]Politis I, Gorewit RC, Muller T, Grosse R: Mammary-derived growth inhibitor protein and messenger ribonucleic acid concentrations in different physiological states of the gland. J Dairy Sci 1992, 75(6):1423-9.
• [77]Clark AJ, Neil C, Gusterson B, McWhir J, Binas B: Deletion of the gene encoding H-FABP/MDGI has no overt effects in the mammary gland. Transgenic Res 2000, 9(6):439-44.
• [78]Bionaz M, Loor JJ: ACSL1, AGPAT6, FABP3, LPIN1, and SLC27A6 are the most abundant isoforms in bovine mammary tissue and their expression is affected by stage of lactation. J Nutr 2008, 138(6):1019-24.
• [79]Buhlmann C, Borchers T, Pollak M, Spener F: Fatty acid metabolism in human breast cancer cells (MCF7) transfected with heart-type fatty acid binding protein. Mol Cell Biochem 1999, 199(1–2):41-8.
• [80]Kadegowda AK, Bionaz M, Piperova LS, Erdman RA, Loor JJ: Peroxisome proliferator-activated receptor-gamma activation and long-chain fatty acids alter lipogenic gene networks in bovine mammary epithelial cells to various extents. J Dairy Sci 2009, 92(9):4276-89.
• [81]Chilliard Y, Ferlay A, Mansbridge RM, Doreau M: Ruminant milk fat plasticity: nutritional control of saturated, polyunsaturated, trans and conjugated fatty acids. Annales De Zootechnie 2000, 49(3):181-205.
• [82]Knudsen J, Grunnet I: Transacylation as a chain-termination mechanism in fatty acid synthesis by mammalian fatty acid synthetase. Synthesis of medium-chain-length (C8-C12) acyl-CoA esters by goat mammary-gland fatty acid synthetase. Biochem J 1982, 202(1):139-43.
• [83]Griinari JM, Corl BA, Lacy SH, Chouinard PY, Nurmela KV, Bauman DE: Conjugated linoleic acid is synthesized endogenously in lactating dairy cows by Delta(9)-desaturase. J Nutr 2000, 130(9):2285-91.
• [84]Corl BA, Baumgard LH, Griinari JM, Delmonte P, Morehouse KM, Yurawecz MP, et al.: Trans-7, cis-9 CLA is synthesized endogenously by delta9-desaturase in dairy cows. Lipids 2002, 37(7):681-8.
• [85]Coleman RA, Mashek DG: Mammalian triacylglycerol metabolism: synthesis, lipolysis, and signaling. Chem Rev 2011, 111(10):6359-86.
• [86]Breckenridge WC, Kuksis A: Structure of bovine milk fat triglycerides. II. Long chain lengths. Lipids 1969, 4(3):197-204.
• [87]Grisart B, Farnir F, Karim L, Cambisano N, Kim JJ, Kvasz A, et al.: Genetic and functional confirmation of the causality of the DGAT1 K232A quantitative trait nucleotide in affecting milk yield and composition. Proc Natl Acad Sci U S A 2004, 101(8):2398-403.
• [88]Bauman DE, Mather IH, Wall RJ, Lock AL: Major advances associated with the biosynthesis of milk. J Dairy Sci 2006, 89(4):1235-43.
• [89]Kao BT, Lewis KA, DePeters EJ, Van Eenennaam AL: Endogenous production and elevated levels of long-chain n-3 fatty acids in the milk of transgenic mice. J Dairy Sci 2006, 89(8):3195-201.
• [90]Kao BT, DePeters EJ, Van Eenennaam AL: Mice raised on milk transgenically enriched with n-3 PUFA have increased brain docosahexaenoic acid. Lipids 2006, 41(6):543-9.
• [91]Watts JL, Browse J: Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2002, 99(9):5854-9.
• [92]Bongiovanni KD, Depeters EJ, Van Eenennaam AL: Neonatal growth rate and development of mice raised on milk transgenically enriched with omega-3 fatty acids. Pediatr Res 2007, 62(4):412-6.
• [93]Wu X, Ouyang H, Duan B, Pang D, Zhang L, Yuan T, et al.: Production of cloned transgenic cow expressing omega-3 fatty acids. Transgenic Res 2012, 21(3):537-43.