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Identification of lipid synthesis and secretion proteins in bovine milk

Published online by Cambridge University Press:  16 January 2014

Jing Lu ,
Toon van Hooijdonk ,
Sjef Boeren ,
Jacques Vervoort  and
Kasper Hettinga
Jing Lu
Affiliation:
Dairy Science and Technology, PDQ group, Wageningen University, Bomenweg 2, 6700 EV, Wageningen, The Netherlands Laboratory of Biochemistry, Wageningen University, Dreijenlaan 3, 6703 HA, Wageningen, The Netherlands
Toon van Hooijdonk
Affiliation:
Dairy Science and Technology, PDQ group, Wageningen University, Bomenweg 2, 6700 EV, Wageningen, The Netherlands
Sjef Boeren
Affiliation:
Laboratory of Biochemistry, Wageningen University, Dreijenlaan 3, 6703 HA, Wageningen, The Netherlands
Jacques Vervoort
Affiliation:
Laboratory of Biochemistry, Wageningen University, Dreijenlaan 3, 6703 HA, Wageningen, The Netherlands
Kasper Hettinga*
Affiliation:
Dairy Science and Technology, PDQ group, Wageningen University, Bomenweg 2, 6700 EV, Wageningen, The Netherlands
*
*For correspondence; e-mail: kasper.hettinga@wur.nl
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Abstract

Lactation physiology is a process that is only partly understood. Proteomics techniques have shown to be useful to help advance the knowledge on lactation physiology in human and rodent species but have not been used as major tools for dairy cows, except for mastitis. In this paper, advanced non-targeted proteomics techniques (Filter aided sample preparation and NanoLC-Orbitrap-MS/MS) were applied to study the milk fat globule membrane and milk serum fraction, resulting in the identification of 246 proteins. Of these, 23 transporters and enzymes were related to lipid synthesis and secretion in mammary gland and their functions are discussed in detail. The identification of these intracellular transporters and enzymes in milk provides a possibility of using milk itself to study lipid synthesis and secretion pathways. This full-scale scan of milk proteins by using non-targeted proteomic analysis helps to reveal the important proteins involved in lipid synthesis and secretion for further examination in targeted studies.

Keywords

Proteomicslipid synthesis and secretionMFGMmilk serum
Type
Research Article
Information
Journal of Dairy Research , Volume 81 , Issue 1 , February 2014 , pp. 65 - 72
Copyright
Copyright © Proprietors of Journal of Dairy Research 2014 

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References

Affolter, M, Grass, L, Vanrobaeys, F, Casado, B & Kussmann, M 2010 Qualitative and quantitative profiling of the bovine milk fat globule membrane proteome. Journal of Proteomics 73 1079–1088 Google Scholar
Aksu, S, Scheler, C, Focks, N, Leenders, F, Theuring, F, Salnikow, J & Jungblut, PR 2002 An iterative calibration method with prediction of post-translational modifications for the construction of a two-dimensional electrophoresis database of mouse mammary gland proteins. Proteomics 2 1452–1463 Google Scholar
Bauman, DE, Mather, IH, Wall, RJ & Lock, AL 2006 Major advances associated with the biosynthesis of milk. Journal of Dairy Science 89 1235–1243 Google Scholar
Beddek, AJ, Rawson, P, Peng, L, Snell, R, Lehnert, K, Ward, HE & Jordan, TW 2008 Profiling the metabolic proteome of bovine mammary tissue. Proteomics 8 1502–1515 Google Scholar
Beigneux, AP, Vergnes, L, Qiao, X, Quatela, S, Davis, R, Watkins, SM, Coleman, RA, Walzem, RL, Philips, M, Reue, K & Young, SG 2006 Agpat6 – a novel lipid biosynthetic gene required for triacylglycerol production in mammary epithelium. Journal of Lipid Research 47 734–744 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. Physiological Genomics 29 312–319 CrossRefGoogle ScholarPubMed
Bionaz, M & Loor, JJ 2008 Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 9 366 Google Scholar
Boehmer, JL, Bannerman, DD, Shefcheck, K & Ward, JL 2008 Proteomic Analysis of Differentially Expressed Proteins in Bovine Milk During Experimentally Induced Escherichia coli Mastitis. Journal of Dairy Science 91 4206–4218 Google Scholar
Boehmer, JL, Ward, JL, Peters, RR, Shefcheck, KJ, McFarland, MA & Bannerman, DD 2010 Proteomic analysis of the temporal expression of bovine milk proteins during coliform mastitis and label-free relative quantification. Journal of Dairy Science 93 593–603 Google Scholar
Bruce Alberts, AJ, Lewis, J, Raff, M, Roberts, K & Walter, P 2002 Molecular Biology of the Cell, 4th edition. New York: Garland Science Google Scholar
Cebo, C, Caillat, H, Bouvier, F & Martin, P 2010 Major proteins of the goat milk fat globule membrane. Journal of Dairy Science 93 868–876 Google ScholarPubMed
Coleman, RA & Lee, DP 2004 Enzymes of triacylglycerol synthesis and their regulation. Progress in Lipid Research 43 134–176 CrossRefGoogle ScholarPubMed
Cox, J & Mann, M 2008 MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology 26 1367–1372 Google Scholar
Cox, J, Neuhauser, N, Michalski, A, Scheltema, RA, Olsen, JV & Mann, M 2011 Andromeda: a peptide search engine integrated into the MaxQuant environment. Journal of Proteome Research 10 1794–1805 Google Scholar
D'Alessandro, A, Zolla, L & Scaloni, A 2011 The bovine milk proteome: cherishing, nourishing and fostering molecular complexity. An interactomics and functional overview. Molecular BioSystems 7 579–597 Google Scholar
D'Amato, A, Bachi, A, Fasoli, E, Boschetti, E, Peltre, G, Sénéchal, H & Righetti, PG 2009 In-depth exploration of cow's whey proteome via combinatorial peptide ligand libraries. Journal of Proteome Research 8 3925–3936 Google Scholar
Davies, CR, Morris, JS, Griffiths, MR, Page, MJ, Pitt, A, Stein, T & Gusterson, BA 2006 Proteomic analysis of the mouse mammary gland is a powerful tool to identify novel proteins that are differentially expressed during mammary development. Proteomics 6 5694–5704 Google Scholar
Dean, PD, Ortiz de Montellano, PR, Bloch, K & Corey, EJ 1967 A soluble 2,3-oxidosqualene sterol cyclase. Journal of Biological Chemistry 242 3014–3015 Google Scholar
Di Vizio, D, Adam, RM, Kim, J, Kim, R, Sotgia, F, Williams, T, Demichelis, F, Solomon, KR, Loda, M, Rubin, MA, Lisanti, MP & Freeman, MR 2008 Caveolin-1 interacts with a lipid raft-associated population of fatty acid synthase. Cell Cycle 7 2257–2267 Google ScholarPubMed
Friedland, N, Liou, HL, Lobel, P & Stock, AM 2003 Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease. Proceedings of the National Academy of Sciences of the United States of America 100 2512–2517 Google Scholar
Glatz, JFC, Luiken, JJFP & Bonen, A 2010 Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiological Reviews 90 367–417 Google Scholar
Hadsell, DL, Olea, W, Wei, J, Fiorotto, ML, Matsunami, RK, Engler, DA & Collier, RJ 2011 Developmental regulation of mitochondrial biogenesis and function in the mouse mammary gland during a prolonged lactation cycle. Physiological Genomics 43 271–285 Google Scholar
Heid, HW & Keenan, TW 2005 Intracellular origin and secretion of milk fat globules. European Journal of Cell Biology 84 245–258 Google Scholar
Heinemann, FS, Korza, G & Ozols, J 2003 A plasminogen-like protein selectively degrades stearoyl-CoA desaturase in liver microsomes. Journal of Biological Chemistry 278 42966–42975 Google Scholar
Hettinga, K, van Valenberg, H, de Vries, S, Boeren, S, van Hooijdonk, T, van Arendonk, J & Vervoort, J 2011 The host defense proteome of human and bovine milk. Plos ONE 6(4) e19433 Google Scholar
Hogarth, CJ, Fitzpatrick, JL, Nolan, AM, Young, FJ, Pitt, A & Eckersall, PD 2004 Differential protein composition of bovine whey: a comparison of whey from healthy animals and from those with clinical mastitis. Proteomics 4 2094–2100 Google Scholar
Huff, MW & Telford, DE 2005 Lord of the rings – the mechanism for oxidosqualene:lanosterol cyclase becomes crystal clear. Trends in Pharmacological Sciences 26 335–340 Google Scholar
Jacobs, JM, Mottaz, HM, Yu, LR, Anderson, DJ, Moore, RJ, Chen, WNU, Auberry, KJ, Strittmatter, EF, Monroe, ME, Thrall, BD, Camp Ii, DG & Smith, RD 2004 Multidimensional proteome analysis of human mammary epithelial cells. Journal of Proteome Research 3 68–75 Google Scholar
Jensen, RG & Pitas, RE 1976 Milk lipoprotein lipases – review. Journal of Dairy Science 59 1203–1214 Google Scholar
Kim, H, Cope, MB, Herring, R, Robinson, G, Wilson, L, Page, GP & Barnes, S 2008 2D difference gel electrophoresis of prepubertal and pubertal rat mammary gland proteomes. Journal of Proteome Research 7 4638–4650 Google Scholar
Larsen, LB, Ravn, P, Boisen, A, Berglund, L & Petersen, TE 1997 Primary structure of EPV20, a secretory glycoprotein containing a previously uncharacterized type of domain. European Journal of Biochemistry 243 437–441 Google Scholar
Long, CA, Patton, S & Mccarthy, RD 1980 Origins of the Cholesterol in Milk. Lipids 15 853–857 Google Scholar
Loor, JJ & Bionaz, M 2008 ACSL1, AGPAT6, FABP3, LPIN1, and SLC27A6 are the most abundant isoforms in bovine mammary tissue and their expression is affected by stage of lactation. Journal of Nutrition 138 1019–1024 Google Scholar
Lu, J, Boeren, S, de Vries, SC, van Valenberg, HJF, Vervoort, J & Hettinga, K 2011 Filter-aided sample preparation with dimethyl labeling to identify and quantify milk fat globule membrane proteins. Journal of Proteomics 75 34–43 CrossRefGoogle ScholarPubMed
Mahley, RW 1988 Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240 622–630 CrossRefGoogle ScholarPubMed
Mather, IH 2000 A review and proposed nomenclature for major proteins of the milk-fat globule membrane. Journal of Dairy Science 83 203–247 Google Scholar
Mather, IH & Keenan, TW 1998 Origin and secretion of milk lipids. Journal of Mammary Gland Biology and Neoplasia 3 259–273 Google Scholar
McManaman, JL & Neville, MC 2003 Mammary physiology and milk secretion. Advanced Drug Delivery Reviews 55 629–641 Google Scholar
McManaman, JL, Russell, TD, Schaack, J, Orlicky, DJ & Robenek, H 2007 Molecular determinants of milk lipid secretion. Journal of Mammary Gland Biology and Neoplasia 12 259–268 Google Scholar
Monks, J, Huey, PU, Hanson, L, Eckel, RH, Neville, MC & Gavigan, S 2001 A lipoprotein-containing particle is transferred from the serum across the mammary epithelium into the milk of lactating mice. Journal of Lipid Research 42 686–696 Google Scholar
Moriya, H, Uchida, K, Okajima, T, Matsuda, T & Nadano, D 2011 Secretion of three enzymes for fatty acid synthesis into mouse milk in association with fat globules, and rapid decrease of the secreted enzymes by treatment with rapamycin. Archives of Biochemistry and Biophysics 508 87–92 Google Scholar
Neville, MC 2006 Lactation and its hormonal control. In Knobil and Neill's Physiology of Reproduction, 3rd edition, pp. 2993–3054 (Ed. Neill, JD). UK: Elsevier Google Scholar
Ohashi, M, Mizushima, N, Kabeya, Y & Yoshimori, T 2003 Localization of mammalian NAD (P) H steroid dehydrogenase-like protein on lipid droplets. Journal of Biological Chemistry 278 36819 Google Scholar
Ollier, S, Chauvet, S, Martin, P, Chilliard, Y & Leroux, C 2008 Goat's αs1-casein polymorphism affects gene expression profile of lactating mammary gland. Animal 2 566–573 Google Scholar
Palmquist, DL 2006 Milk fat: origin of fatty acids and influence of nutritional factors thereon. In Advanced Dairy Chemistry, Volume 2: Lipids, 3rd edition, pp. 43–92 (Ed. Fox, PF & McSweeney, PLH). USA: Springer Google Scholar
Popjak, G, French, TH & Folley, SJ 1951 Utilization of acetate for milk-fat synthesis in the lactating goat. Biochemical Journal 48 411–416 Google Scholar
Reinhardt, TA & Lippolis, JD 2006 Bovine milk fat globule membrane proteome. Journal of Dairy Research 73 406–416 Google Scholar
Reinhardt, TA & Lippolis, JD 2008 Developmental changes in the milk fat globule membrane proteome during the transition from colostrum to milk. Journal of Dairy Science 91 2307–2318 Google Scholar
Schwenk, RW, Holloway, GP, Luiken, JJFP, Bonen, A & Glatz, JFC 2010 Fatty acid transport across the cell membrane: regulation by fatty acid transporters. Prostaglandins Leukotrienes and Essential Fatty Acids 82 149–154 Google Scholar
Smith, PK, Krohn, RI, Hermanson, GT, Mallia, AK, Gartner, FH, Provenzano, MD, Fujimoto, EK, Goeke, NM, Olson, BJ & Klenk, DC 1985 Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150 76–85 Google Scholar
Smolenski, G, Haines, S, Kwan, FYS, Bond, J, Farr, V, Davis, SR, Stelwagen, K & Wheeler, TT 2007 Characterisation of host defence proteins in milk using a proteomic approach. Journal of Proteome Research 6 207–215 Google Scholar
Stock, AM, Xu, S, Benoff, B, Liou, HL & Lobel, P 2007 Structural basis of sterol binding by NPC2, a lysosomal protein deficient in Niemann-Pick type C2 disease. Journal of Biological Chemistry 282 23525–23531 Google Scholar
Suchyta, SP, Sipkovsky, S, Halgren, RG, Kruska, R, Elftman, M, Weber-Nielsen, M, Vandehaar, MJ, Xiao, L, Tempelman, RJ & Coussens, PM 2004 Bovine mammary gene expression profiling using a cDNA microarray enhanced for mammary-specific transcripts. Physiological Genomics 16 8–18 Google Scholar
Wiśniewski, JR, Zougman, A, Nagaraj, N & Mann, M 2009 Universal sample preparation method for proteome analysis. Nature Methods 6 359–362 Google ScholarPubMed
Wu, CC, Howell, KE, Neville, MC, Yates Iii, JR & McManaman, JL 2000 Proteomics reveal a link between the endoplasmic reticulum and lipid secretory mechanisms in mammary epithelial cells. Electrophoresis 21 3470–3482 3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Yeagle, P 1991 Modulation of membrane function by cholesterol. Biochimie 73 1303–1310 Google Scholar
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