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Department of Animal Science, Cornell University, Ithaca, NY 14853
4To whom correspondence should be addressed. E-mail: deb6{at}cornell.edu.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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-casein. The reductions in mRNA were also correlated with the appearance of trans-10, cis-12 CLA in the milk fat for ACC, FAS, lipoprotein lipase and GPAT. This study demonstrates that diet-induced MFD involves coordinated effects on mRNA for mammary lipid synthesis pathways, and provides support for a mechanism involving alterations in transcriptional activation of these genes.
KEY WORDS: • conjugated linoleic acid • milk fat • fatty acid synthesis • lipogenic genes • metabolomics
The fat content and fatty acid composition of milk can be dramatically affected by dietary manipulation in many species (1,2). This has been studied extensively in ruminants; one striking example is the low fat milk syndrome, commonly referred to as milk fat depression (MFD).4 In this situation, high concentrate/low forage (HC/LF) diets or dietary supplements of plant oils or fish oils cause a dramatic decline in milk fat secretion, whereas yields of milk and other milk components remain unchanged [for reviews, see (3–5)]. First recognized by Boussingault in 1845 (6), this phenomenon involves an interaction between alterations in rumen digestion and tissue metabolism. Although many theories have been proposed to explain the basis of MFD, its mechanism has remained elusive [for reviews, see (3,4)]. Recent investigations have shown that a reduction in activities and/or mRNA for fatty acid synthase (FAS), acetyl-CoA carboxylase (ACC) and stearoyl-CoA desaturase (SCD) occurred in mammary tissue when MFD was induced by plant (7) or fish oil (8) supplements. However, these studies were limited in scope, and there have been no similar investigations of MFD induced by the classical HC/LF diet.
Bauman and Griinari (3) proposed that alterations in rumen biohydrogenation of PUFA during MFD resulted in the production of unique fatty acid intermediates that are absorbed and elicit direct inhibitory effects on milk fat synthesis. This is referred to as the biohydrogenation theory and support comes from studies demonstrating that trans-10, cis-12 conjugated linoleic acid (CLA) is a potent inhibitor of milk fat synthesis and secretion (9–11). Under conditions of diet-induced MFD, the rumen production and milk fat content of trans-10, cis-12 CLA increases (3,7,12). Baumgard et al. (13) recently demonstrated that abomasal infusion of pure trans-10, cis-12 CLA was associated with a dramatic reduction in milk fat secretion and coordinate reductions in mRNA abundance for a number of key genes involved in the biosynthesis of milk fat. However, these coordinated effects on mammary lipid synthesis genes have not been demonstrated in the case of the classical HC/LF diet-induced MFD or MFD induced by any dietary means.
The objectives of the present study were to relate MFD induced by feeding a HC/LF diet to the milk fat content of trans-10, cis-12 CLA, and to determine whether this treatment would lead to coordinate reductions in mammary abundance of mRNA for genes involved in the various pathways of milk fat synthesis. Specific genes examined included those for lipogenic enzymes involved in de novo synthesis, uptake and transport of preformed fatty acids, desaturation and formation of milk fat triglycerides.
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MATERIALS AND METHODS |
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All procedures were approved by the Cornell University Institutional Animal Care and Use Committee. Lactating Holstein cows (n = 3; 111 ± 12 d postpartum, mean ± SD) were used in a single reversed design; two cows were fed the control diet and one was fed the HC/LF diet in the first experimental period and treatments were reversed in the second period. Cows were housed in individual tie-stalls at the Cornell University Teaching and Research Center (Harford, NY) during the experimental periods and at the Large Animal Research and Teaching Unit at Cornell University (Ithaca, NY) for surgeries and recovery periods.
Diets were formulated using the Cornell Net Carbohydrate and Protein System (14) to meet or exceed nutrient requirements (15) (Table 1). Treatment periods were 3 wk with an intervening 3-wk recovery interval between periods. Cows consumed feed ad libitum with fresh feed given once daily and had access to fresh water at all times. Feed was sampled weekly and dried at 50°C for 72 h for determination of dry matter. Weekly feed samples were composited for each period and composition determined by wet chemistry methods (16) (Dairy One Cooperative, Ithaca, NY).
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Fatty acid analysis.
Composited milk samples were centrifuged at 17,800 x g for 30 min at 8°C and 300–400 mg of fat cake was removed for extraction and methylation. Lipid extraction was performed according to Hara and Radin (17) and methyl esters of the fatty acids were prepared by transesterification with sodium methoxide according to the method of Christie (18) as detailed by Chouinard et al. (19). FAME were quantified by GC using a SP-2560 capillary column (100 m x 0.25 mm i.d. with 0.2-µm film thickness; Supelco, Bellefonte, PA). The analysis involved a programmed run with temperature ramps. The oven temperature was initially 50°C for 1 min then ramped to 160°C at 5°C/min and held for 42 min. The temperature was then ramped again at 5°C/min to 190°C and held for 22 min. Injector and detector temperatures were maintained at 250°C. The flow rate for hydrogen carrier gas was 1 mL/min. Hydrogen flow to the detector was 25 mL/min, air flow was 400 mL/min and the nitrogen make-up gas flow was 45 mL/min.
Each peak was identified and quantified using pure methyl ester samples (Nu-Chek-Prep, Elysian, MN). A butter reference standard (CRM 164; Commission of the European Communities, Community Bureau of Reference, Brussels, Belgium) was used to determine recoveries and correction factors for individual fatty acids. The butter reference standard was analyzed at regular intervals throughout the GC analyses as an aid in quality control.
Tissue biopsy and analysis.
On the last day of each treatment period, 
500 mg of mammary tissue was obtained by surgical biopsy from the midpoint section of a rear quarter according to the method of Farr et al. (20). Modifications and surgical procedures for the biopsy and postsurgery care were described previously (13).
Tissue biopsies were snap-frozen in liquid nitrogen and transported to the laboratory where they were kept at -80°C until used for RNA extraction. Total RNA was extracted from mammary tissue by the method of Chomczynski and Sacchi (21). Total RNA (25 µg) from each sample was separated by 1% agarose-formaldehyde gel electrophoresis, transferred to GeneScreen membranes (DuPont NEN, Boston, MA) by capillary blotting and hybridized with 32P-dCTP–labeled cDNA probes at 45°C overnight. Probes used for hybridization were obtained as follows: ovine ACC and SCD cDNAs were provided by M. T. Travers and M. C. Barber (Hannah Research Institute, Ayr, UK); ovine FAS and -casein (KCAS) cDNAs from C. Leroux and J. Mercier, respectively (LGBC-INRA, Jouy-en-Josas, France); bovine expressed sequence tags with homology to lipoprotein lipase (LPL), glycerol phosphate acyltransferase (GPAT), acylglycerol phosphate acyltransferase (AGPAT) and fatty acyl-CoA ligase (FACL) were obtained from J. C. Byatt (Monsanto, St. Louis, MO); human cDNA for cytosolic fatty acid binding protein (FABP) was purchased from the American Type Culture Collection (Manassas, VA); and ß-actin cDNA was obtained from Superarray (Bethesda, MD). Expression of all analyzed genes was quantified with a Fujix Bio-Imaging Analyzer BAS 1000 phosphoimager (Fuji Medical Systems, Stamford, CT) and were normalized to the expression of ß-actin mRNA.
Statistical analysis.
Treatment effects on animal performance, milk fatty acid composition and mRNA abundance were analyzed using the General Linear Models procedure of SAS (SAS Institute, Cary, NC). Bonferroni t tests were used to assess differences between treatments. Relation of differences in mRNA abundance to trans-10, cis-12 CLA content of milk fat was performed using the regression procedure of SAS. Differences were considered significant when P < 0.05.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The biohydrogenation theory of MFD proposes that unique fatty acid intermediates produced by altered rumen biohydrogenation are causally related to diet-induced MFD (3). One example is trans-10, cis-12 CLA, and studies have established that this CLA isomer is a potent inhibitor of milk fat synthesis in dairy cows (9,10,11,22). In the present study, we observed that consumption of the HC/LF diet increased the concentration of trans-10, cis-12 CLA in the milk fat. However, other biohydrogenation intermediates in addition to trans-10, cis-12 CLA may be involved in causing the observed decrease in milk fat (4). We provided an initial evaluation of this by using the dose-response curve relating milk fat content of trans-10, cis-12 CLA to milk fat yield during abomasal infusion of relatively pure trans-10, cis-12 CLA (11). Comparison of this response curve with the milk fat content of trans-10, cis-12 CLA and the reduction in milk fat observed during diet-induced MFD in the present study and other published studies (7,12) indicates a divergence in the relationship (Fig. 3). This strongly implies that there must be additional, unidentified fatty acid intermediates inhibiting milk fat synthesis during diet-induced MFD. The milk fat content of trans-10 18:1 also increased markedly when cows were fed the HC/LF diet (Table 3), and similar increases were observed for other types of diet-induced MFD (7,23,24). This fatty acid is also a rumen biohydrogenation intermediate and is formed from the reduction of the cis-12 double bond in trans-10, cis-12 CLA (25). However, the availability of trans-10 18:1 for experimental use is limited and there have been no studies that directly examined its role in the reduction in milk fat associated with diet-induced MFD. If trans-10 18:1 does inhibit milk fat synthesis, its potency must be substantially less than that of trans-10, cis-12 CLA based on results from studies using partially hydrogenated vegetable oils to cause MFD [see discussion in (4)].
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The mammary changes observed in cows exhibiting MFD in the present study are consistent with previous investigations of diet-induced MFD, although those studies were very limited in scope. Opstvedt et al. (26) reported that mammary activity of FAS tended to be reduced in cows fed a HC/LF diet. Piperova et al. (7) demonstrated that feeding a low fiber diet supplemented with soybean oil caused MFD and reduced mammary abundance of ACC mRNA and ACC and FAS enzyme activity. Cows fed a fish oil supplement to cause MFD also exhibited reduced mammary transcript abundance for FAS, ACC and SCD with less clear effects on LPL (8). In a more comprehensive study, Baumgard et al. (13) showed that mammary tissue from cows administered abomasally infused trans-10, cis-12 CLA to induce MFD exhibited reductions in mRNA abundance for genes involved in uptake and transport (LPL, FABP), de novo synthesis (ACC and FAS), desaturation (SCD) and triglyceride synthesis (GPAT).
This is the first investigation to demonstrate the coordinated nature of the effects on lipid synthesis genes in diet-induced MFD. These coordinated changes, in combination with the lack of effect on unrelated genes such as KCAS, suggest that the effects of a MFD diet will be mediated through a pathway-specific controller of gene expression. A logical candidate for this control is the sterol response element-binding protein (SREBP) family of transcription factors (27), and we have recently linked alterations in the SREBP regulatory pathway to treatment of bovine mammary cells with trans-10, cis-12 CLA (28). The observed effects on mRNA abundance could also be due to alterations in mRNA stability, and this was not examined in the present study. Other, shorter-term mechanisms such as direct enzyme inhibition could result in a feedback downregulation on gene expression, and the present study does not exclude this possibility. However, it seems likely that if one pathway involved in lipid synthesis were acutely affected in such a manner (i.e., de novo synthesis), other pathways would be upregulated to compensate (i.e., uptake and transport of preformed fatty acids from circulation).
The present study demonstrated that diet-induced MFD resulted in a coordinated reduction in mRNA abundance for genes associated with all major aspects of mammary lipid synthesis in dairy cows, and these reductions were related to the appearance of trans-10, cis-12 CLA in milk fat. Comparison with dose response relationships obtained from abomasal infusion of pure trans-10, cis-12 CLA suggests that there may be other unique biohydrogenation intermediates also contributing to the inhibition of milk fat synthesis in the mammary gland during diet-induced MFD. Further research targeted at identifying the mechanism by which these reductions occur and the possible involvement of central coordinators of metabolism such as SREBP will be useful in fully characterizing diet-induced milk fat depression, a phenomenon that has been under investigation for over 150 years.
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FOOTNOTES |
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2 Supported in part by the National Research Initiative Competitive Grants Program, Cooperative State Research, Education, and Extension Service, United States Department of Agriculture (#2003–35206–12819), Northeast Dairy Foods Research Center and Cornell Agricultural Experiment Station.
3 Present address: Animal Science Department, California Polytechnic State University, San Luis Obispo, CA 93407.
5 Abbreviations used: ACC, acetyl CoA carboxylase; AGPAT, acylglycerol phosphate acyl transferase; CLA, conjugated linoleic acid; FABP, fatty acid binding protein; FACL, fatty acyl CoA ligase; FAS, fatty acid synthase; GPAT, glycerol phosphate acyl transferase; HC/LF, high concentrate/low forage; KCAS, -casein; LPL, lipoprotein lipase; MFD, milk fat depression; SCD, stearoyl-CoA desaturase; SREBP, sterol response element binding protein.
Manuscript received 19 June 2003. Initial review completed 18 July 2003. Revision accepted 29 July 2003.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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20. Farr, V. C., Stelwagen, K., Cate, L. R., Molenaar, A. J., McFadden, T. B. & Davis, S. R. (1996) An improved method for the routine biopsy of bovine mammary tissue. J. Dairy Sci. 79:543-549.[Abstract]
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23. Offer, N. W., Marsden, M., Dixon, J., Speake, B. K. & Thacker, F. E. (1999) Effect of dietary fat supplements on levels of n-3 polyunsaturated fatty acids, trans acids and conjugated linoleic acid in bovine milk. Anim. Sci. 69:613-625.
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25. Griinari, J. M. & Bauman, D. E. (1999) Biosynthesis of conjugated linoleic acid and its incorporation into meat and milk in ruminants. Yurawecz, M. P. Mossoba, M. M. Kramer, J.K.G. Pariza, M. W. Nelson, G. J. eds. Advances in Conjugated Linoleic Acid Research, Volume 1 1999:180-200 AOCS Press Champaign, IL. .
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0.01, **P 