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Sustained upregulation of stearoyl-CoA desaturase in bovine mammary tissue with contrasting changes in milk fat synthesis and lipogenic gene networks caused by lipid supplements

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Abstract

Long-term mammary expression patterns of lipogenic gene networks due to dietary lipid remain largely unknown. Mammary tissue was biopsied for transcript profiling of 29 genes at 0, 7, and 21 days of feeding cows saturated lipid (EB100) or a blend of fish/soybean oil (FSO) to depress milk fat. Milk fat yield decreased gradually with FSO and coincided with lower molar yield of fatty acids synthesized de novo, stearic acid, and oleic acid. The PPARγ targets LPIN1 and SREBF1 along with ACSS2, ACACA, FASN, and LPL increased by day 7 of feeding EB100, but differences between diets disappeared by day 21. Expression of SCAP increased markedly over time with FSO and differed from EB100 by approximately sevenfold on day 21. Expression of THRSP decreased by day 7 with both diets and returned to basal levels by day 21. SCD expression increased linearly through 7 days and remained elevated with both diets, a likely mechanism to ensure the proper level of endogenous oleic acid via desaturation of dietary stearate (EB100) or via more SCD protein to account for the reduction in stearate supply from the rumen (FSO). Despite this response, endogenous oleate was insufficient to restore normal milk fat synthesis. Only 2 of 29 genes differed in expression between diets on day 21, suggesting that transcriptional control mechanisms regulating fat synthesis were established as early as 7 days post-feeding. Gene expression reflected vastly different physiological responses by mammary tissue to adjust its metabolism to the influx of saturated fatty acids, trans10-18:1, and/or to the lack of stearic acid.

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References

  • Ahnadi CE, Beswick N, Delbecchi L, Kennelly JJ, Lacasse P (2002) Addition of fish oil to diets for dairy cows. II. Effects on milk fat and gene expression of mammary lipogenic enzymes. J Dairy Res 69:521–31

    Article  CAS  PubMed  Google Scholar 

  • Bionaz M, Loor JJ (2007) Identification of reference genes for quantitative real-time PCR in the bovine mammary gland during the lactation cycle. Physiol Genomics 29:312–9

    Article  CAS  PubMed  Google Scholar 

  • Bionaz M, Loor JJ (2008a) 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 138:1019–1024

    CAS  PubMed  Google Scholar 

  • Bionaz M, Loor JJ (2008b) Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 9:366

    Article  PubMed  Google Scholar 

  • Bitman J, Wood DL (1990) Changes in milk fat phospholipids during lactation. J Dairy Sci 73:1208–16

    Article  CAS  PubMed  Google Scholar 

  • Bobrovnikova-Marjon E, Hatzivassiliou G, Grigoriadou C, Romero M, Cavener DR, Thompson CB, Diehl JA (2008) PERK-dependent regulation of lipogenesis during mouse mammary gland development and adipocyte differentiation. Proc Natl Acad Sci U S A 105:16314–16319

    Article  CAS  PubMed  Google Scholar 

  • Desvergne B, Michalik L, Wahli W (2006) Transcriptional regulation of metabolism. Physiol Rev 86:465–514

    Article  CAS  PubMed  Google Scholar 

  • Engelking LJ, Kuriyama H, Hammer RE, Horton JD, Brown MS, Goldstein JL, Liang G (2004) Overexpression of Insig-1 in the livers of transgenic mice inhibits SREBP processing and reduces insulin-stimulated lipogenesis. J Clin Invest 113:1168–1175

    CAS  PubMed  Google Scholar 

  • Fielding BA, Frayn KN (1998) Lipoprotein lipase and the disposition of dietary fatty acids. Br J Nutr 80:495–502

    CAS  PubMed  Google Scholar 

  • Foufelle F, Ferre P (2002) New perspectives in the regulation of hepatic glycolytic and lipogenic genes by insulin and glucose: a role for the transcription factor sterol regulatory element binding protein-1c. Biochem J 366:377–391

    Article  CAS  PubMed  Google Scholar 

  • Garnsworthy PC, Masson LL, Lock AL, Mottram TT (2006) Variation of milk citrate with stage of lactation and de novo fatty acid synthesis in dairy cows. J Dairy Sci 89:1604–12

    Article  CAS  PubMed  Google Scholar 

  • Harvatine KJ, Bauman DE (2006) SREBP1 and thyroid hormone responsive spot 14 (S14) are involved in the regulation of bovine mammary lipid synthesis during diet-induced milk fat depression and treatment with CLA. J Nutr 136:2468–2474

    CAS  PubMed  Google Scholar 

  • Horton JD, Goldstein JL, Brown MS (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109:1125–1131

    CAS  PubMed  Google Scholar 

  • Huffman TA, Mothe-Satney I, Lawrence JC Jr (2002) Insulin-stimulated phosphorylation of lipin mediated by the mammalian target of rapamycin. Proc Natl Acad Sci U S A 99:1047–1052

    Article  CAS  PubMed  Google Scholar 

  • Invernizzi G, Thering BJ, Bionaz M, Graugnard D, Piantoni P, Everts RE, Lewin HA, Savoini G, Loor JJ (2009) New insights on mammary tissue responses to dietary lipids using transcriptomics. Proceedings of the XIth International Symposium on Ruminant Physiology, Clermont-Ferrand, France, September 6–9, pp 540–542

  • Ishimoto K, Nakamura H, Tachibana K, Yamasaki D, Ota A, Hirano K, Tanaka T, Hamakubo T, Sakai J, Kodama T, Doi T (2009) Sterol-mediated regulation of human lipin 1 gene expression in hepatoblastoma cells. J Biol Chem 284:22195–22205

    Article  CAS  PubMed  Google Scholar 

  • Kadegowda AK, Bionaz M, Piperova LS, Erdman RA, Loor JJ (2009a) 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 92:4276–4289

    Article  CAS  PubMed  Google Scholar 

  • Kadegowda AK, Bionaz M, Thering B, Piperova LS, Erdman RA, Loor JJ (2009b) Identification of internal control genes for quantitative polymerase chain reaction in mammary tissue of lactating cows receiving lipid supplements. J Dairy Sci 92:2007–19

    Article  CAS  PubMed  Google Scholar 

  • Kast-Woelbern HR, Dana SL, Cesario RM, Sun L, de Grandpre LY, Brooks ME, Osburn DL, Reifel-Miller A, Klausing K, Leibowitz MD (2004) Rosiglitazone induction of insig-1 in white adipose tissue reveals a novel interplay of peroxisome proliferator-activated receptor gamma and sterol regulatory element-binding protein in the regulation of adipogenesis. J Biol Chem 279:23908–23915

    Article  CAS  PubMed  Google Scholar 

  • Keenan TW, Huang CM (1972) Membranes of mammary gland. VI. Lipid and protein composition of Golgi apparatus and rough endoplasmic reticulum from bovine mammary gland. J Dairy Sci 55:1586–96

    Article  CAS  PubMed  Google Scholar 

  • Lee AH, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23:7448–7459

    Article  CAS  PubMed  Google Scholar 

  • Legrand P, Catheline D, Fichot MC, Lemarchal P (1997) Inhibiting delta9-desaturase activity impairs triacylglycerol secretion in cultured chicken hepatocytes. J Nutr 127:249–56

    CAS  PubMed  Google Scholar 

  • Loor JJ, Herbein JH (2003) Reduced fatty acid synthesis and desaturation due to exogenous trans10, cis12-CLA in cows fed oleic or linoleic oil. J Dairy Sci 86:1354–1369

    Article  CAS  PubMed  Google Scholar 

  • Loor JJ, Doreau M, Chardigny JM, Ollier A, Sebedio JL, Chilliard Y (2005a) Effects of ruminal or duodenal supply of fish oil on milk fat secretion and profiles of trans-fatty acids and conjugated linoleic acid isomers in dairy cows fed maize silage. Anim Feed Sci Technol 119:227–246

    Article  CAS  Google Scholar 

  • Loor JJ, Ueda K, Ferlay A, Chilliard Y, Doreau M (2005b) Intestinal flow and digestibility of trans fatty acids and conjugated linoleic acids (CLA) in dairy cows fed a high-concentrate diet supplemented with fish oil, linseed oil, or sunflower oil. Anim Feed Sci Technol 119:203–225

    Article  CAS  Google Scholar 

  • Mandl J, Meszaros T, Banhegyi G, Hunyady L, Csala M (2009) Endoplasmic reticulum: nutrient sensor in physiology and pathology. Trends Endocrinol Metab 20:194–201

    Article  CAS  PubMed  Google Scholar 

  • Miyazaki M, Kim YC, Ntambi JM (2001) A lipogenic diet in mice with a disruption of the stearoyl-CoA desaturase 1 gene reveals a stringent requirement of endogenous monounsaturated fatty acids for triglyceride synthesis. J Lipid Res 42:1018–1024

    CAS  PubMed  Google Scholar 

  • Miyazaki M, Dobrzyn A, Man WC, Chu K, Sampath H, Kim HJ, Ntambi JM (2004) Stearoyl-CoA desaturase 1 gene expression is necessary for fructose-mediated induction of lipogenic gene expression by sterol regulatory element-binding protein-1c-dependent and -independent mechanisms. J Biol Chem 279:25164–71

    Article  CAS  PubMed  Google Scholar 

  • Mosley EE, Shafii Dagger B, Moate PJ, McGuire MA (2006) cis-9, trans-11 conjugated linoleic acid is synthesized directly from vaccenic acid in lactating dairy cattle. J Nutr 136:570–575

    CAS  PubMed  Google Scholar 

  • Offer NW, Marsden M, Phipps RH (2001) Effect of oil supplementation of a diet containing a high concentration of starch on levels of trans fatty acids and conjugated linoleic acids in bovine milk. Anim Sci 73:533–540

    CAS  Google Scholar 

  • Pegorier JP, Le May C, Girard J (2004) Control of gene expression by fatty acids. J Nutr 134:2444S–2449S

    CAS  PubMed  Google Scholar 

  • Peterson DG, Matitashvili EA, Bauman DE (2004) The inhibitory effect of trans-10, cis-12 CLA on lipid synthesis in bovine mammary epithelial cells involves reduced proteolytic activation of the transcription factor SREBP-1. J Nutr 134:2523–2527

    CAS  PubMed  Google Scholar 

  • Piperova LS, Teter BB, Bruckental I, Sampugna J, Mills SE, Yurawecz MP, Fritsche J, Ku K, Erdman RA (2000) Mammary lipogenic enzyme activity, trans fatty acids and conjugated linoleic acids are altered in lactating dairy cows fed a milk fat-depressing diet. J Nutr 130:2568–74

    CAS  PubMed  Google Scholar 

  • Postic C, Dentin R, Denechaud PD, Girard J (2007) ChREBP, a transcriptional regulator of glucose and lipid metabolism. Annu Rev Nutr 27:179–192

    Article  CAS  PubMed  Google Scholar 

  • Reue K, Zhang P (2008) The lipin protein family: dual roles in lipid biosynthesis and gene expression. FEBS Lett 582:90–96

    Article  CAS  PubMed  Google Scholar 

  • Sampath H, Miyazaki M, Dobrzyn A, Ntambi JM (2007) Stearoyl-CoA desaturase-1 mediates the pro-lipogenic effects of dietary saturated fat. J Biol Chem 282:2483–93

    Article  CAS  PubMed  Google Scholar 

  • Shingfield KJ, Reynolds CK, Hervas G, Griinari JM, Grandison AS, Beever DE (2006) Examination of the persistency of milk fatty acid composition responses to fish oil and sunflower oil in the diet of dairy cows. J Dairy Sci 89:714–732

    Article  CAS  PubMed  Google Scholar 

  • Shingfield KJ, Bernard L, Leroux C, Chilliard Y (2010) Role of trans fatty acids in the nutritional regulation of mammary lipogenesis in ruminants. Animal 4:1140–1166

    Google Scholar 

  • Thering BJ, Graugnard DE, Piantoni P, Loor JJ (2009) Adipose tissue lipogenic gene networks due to lipid feeding and milk fat depression in lactating cows. J Dairy Sci 92:4290–300

    Article  CAS  PubMed  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034

    Article  PubMed  Google Scholar 

  • Verheijen MH, Camargo N, Verdier V, Nadra K, de Preux Charles AS, Médard JJ, Luoma A, Crowther M, Inouye H, Shimano H, Chen S, Brouwers JF, Helms JB, Feltri ML, Wrabetz L, Kirschner D, Chrast R, Smit AB (2009) SCAP is required for timely and proper myelin membrane synthesis. Proc Natl Acad Sci U S A 106:21383–8

    Article  CAS  PubMed  Google Scholar 

  • Worgall TS (2007) Sphingolipids: major regulators of lipid metabolism. Curr Opin Clin Nutr Metab Care 10:149–155

    Article  CAS  PubMed  Google Scholar 

  • Yang SL, Bu DP, Wang JQ, Hu ZY, Li D, Wei HY, Zhou LY, Loor JJ (2009) Soybean oil and linseed oil supplementation affect profiles of ruminal microorganisms in dairy cows. Animal 11:1562–1569

    Article  Google Scholar 

  • Zierath JR (2007) The path to insulin resistance: paved with ceramides? Cell Metab 5:161–163

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Supported by the Cooperative State Research, Education, and Extension Service, USDA, under Hatch projects ILLU-538-307 and ILLU-538-391 (both to JJL). We gratefully acknowledge the input and help of Dr. Massimo Bionaz (University of Illinois, Urbana) during the development of the manuscript. The fish oil used in this study was donated by Omega Protein and the soybean oil by Archer Daniels Midland (Decatur, IL, USA). EnergyBooster 100 was a gift from Milk Specialties Inc. (Dundee, IL, USA). We are also grateful for the help from the staff of the University of Illinois Dairy Research and Teaching Unit for animal care.

Integrity of research and reporting

The authors declare that the experiment complies with the current laws of the USA. The authors declare no conflicts of interest.

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Authors and Affiliations

  1. Mammalian NutriPhysioGenomics, Department of Animal Sciences, University of Illinois, Urbana, IL, 61801, USA

    Guido Invernizzi, Betsy J. Thering & Juan J. Loor

  2. Division of Nutritional Sciences, University of Illinois, Urbana, IL, 61801, USA

    Guido Invernizzi, Betsy J. Thering & Juan J. Loor

  3. Department of Veterinary Science and Technology for Food Safety, Faculty of Veterinary Medicine, University of Milan, Milan, Italy

    Guido Invernizzi & Giovanni Savoini

  4. Department of Animal and Veterinary Science, University of Idaho, Moscow, ID, 83844, USA

    Mark A. McGuire

Authors
  1. Guido Invernizzi
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  2. Betsy J. Thering
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  3. Mark A. McGuire
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  4. Giovanni Savoini
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  5. Juan J. Loor
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Corresponding author

Correspondence to Juan J. Loor.

Additional information

Guido Invernizzi and Betsy J. Thering contributed equally.

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Online Resource 1 (Microsoft Word)

The file contains additional materials and methods and additional results and discussion. Measurements and sample collection; biopsies and RNA extraction; quantitative PCR, primer design, and primer testing; quantitative PCR performance; diet nutrient composition; fatty acid composition of lipid supplements; gene expression results across all treatments at the end of the study; longitudinal production data; longitudinal milk fatty acid profiles. (DOC 2626 kb)

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Invernizzi, G., Thering, B.J., McGuire, M.A. et al. Sustained upregulation of stearoyl-CoA desaturase in bovine mammary tissue with contrasting changes in milk fat synthesis and lipogenic gene networks caused by lipid supplements. Funct Integr Genomics 10, 561–575 (2010). https://doi.org/10.1007/s10142-010-0179-y

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  • DOI: https://doi.org/10.1007/s10142-010-0179-y

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