Quantitative analysis of the human milk whey proteome reveals developing milk and Mammary-Gland functions across the first year of lactation

Proteomes

Volumn 1, Issue 2, 2013, Pages 128-158

  Zhang, Qiang ^a   Cundiff, Judy K ^a   Maria, Sarah D ^a   McMahon, Robert J ^a   Woo, Jessica G ^b   Davidson, Barbara S ^b   Morrow, Ardythe L ^b  

^a Mead Johnson Nutrition   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Cellular processes; Complement system; Human milk; Immunoglobulins; Milk proteins

Indexed keywords

EID: 84893863185     PISSN: None     EISSN: 22277382     Source Type: Journal    
DOI: 10.3390/proteomes1020128     Document Type: Article

References (71)

1. Zhang, Q.; Carpenter, C.J. Proteomics in milk and milk processing. In Proteomics in Foods; Toldrá, F., Nollet, L.M.L., Eds.; Springer: New York, NY, USA, 2013; pp. 223-245
2. Bauman, D.E.; Mather, I.H.; Wall, R.J.; Lock, A.L. Major advances associated with the biosynthesis of milk. J. Dairy Sci. 2006, 89, 1235-1243
3. Ollier, S.; Robert-Granie, C.; Bernard, L.; Chilliard, Y.; Leroux, C. Mammary transcriptome analysis of food-deprived lactating goats highlights genes involved in milk secretion and programmed cell death. J. Nutr. 2007, 137, 560-567
4. Bionaz, M.; Loor, J.J. Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 2008, 9, e366
5. Bionaz, M.; Loor, J.J. Ruminant metabolic systems biology: Reconstruction and integration of Transcriptome dynamics underlying functional responses of tissues to nutrition and physiological state. Gene Regul. Syst. Biol. 2012, 6, 109-125
6. Elsik, C.G.; Tellam, R.L.; Worley, K.C.; Gibbs, R.A.; Muzny, D.M.; Weinstock, G.M.; Adelson, D.L.; Eichler, E.E.; Elnitski, L.; Guigo, R.; et al. The genome sequence of taurine cattle: A window to ruminant biology and evolution. Science 2009, 324, 522-528
7. Heid, H.W.; Keenan, T.W. Intracellular origin and secretion of milk fat globules. Eur. J. Cell Biol. 2005, 84, 245-258
8. Heird, W.C.; Schwarz, S.M.; Hansen, I.H. Colostrum-induced enteric mucosal growth in beagle puppies. Pediatr. Res. 1984, 18, 512-515
9. Goldman, A.S. The immune system of human milk: Antimicrobial, antiinflammatory and immunomodulating properties. Pediatr. Infect. Dis. J. 1993, 12, 664-671
10. Hamosh, M. Bioactive factors in human milk. Pediatr. Clin. North Am. 2001, 48, 69-86
11. Karhumaa, P.; Leinonen, J.; Parkkila, S.; Kaunisto, K.; Tapanainen, J.; Rajaniemi, H. The identification of secreted carbonic anhydrase VI as a constitutive glycoprotein of human and rat milk. Proc. Natl. Acad. Sci. USA 2001, 98, 11604-11608
12. Frid, A.H.; Nilsson, M.; Holst, J.J.; Bjorck, I.M. Effect of whey on blood glucose and insulin responses to composite breakfast and lunch meals in type 2 diabetic subjects. Am. J. Clin. Nutr. 2005, 82, 69-75
13. Schack-Nielsen, L.; Michaelsen, K.F. Advances in our understanding of the biology of human milk and its effects on the offspring. J. Nutr. 2007, 137, 503S-510S
14. Pal, S.; Ellis, V. Acute effects of whey protein isolate on blood pressure, vascular function and inflammatory markers in overweight postmenopausal women. Br. J. Nutr. 2011, 105, 1512-1519
15. Zivkovic, A.M.; German, J.B.; Lebrilla, C.B.; Mills, D.A. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc. Natl. Acad. Sci. USA 2011, 108, 4653-4658
16. Fortunato, D.; Giuffrida, M.G.; Cavaletto, M.; Garoffo, L.P.; Dellavalle, G.; Napolitano, L.; Giunta, C.; Fabris, C.; Bertino, E.; Coscia, A.; et al. Structural proteome of human colostral fat globule membrane proteins. Proteomics 2003, 3, 897-905
17. Cavaletto, M.; Giuffrida, M.G.; Conti, A. The proteomic approach to analysis of human milk fat globule membrane. Clin. Chim. Acta 2004, 347, 41-48
18. Palmer, D.J.; Kelly, V.C.; Smit, A.M.; Kuy, S.; Knight, C.G.; Cooper, G.J. Human colostrum: Identification of minor proteins in the aqueous phase by proteomics. Proteomics 2006, 6, 2208-2216
19. Mangé, A.; Bellet, V.; Tuaillon, E.; van de Perre, P.; Solassol, J. Comprehensive proteomic analysis of the human milk proteome: Contribution of protein fractionation. J. Chromatogr. B 2008, 876, 252-256
20. Picariello, G.; Ferranti, P.; Mamone, G.; Roepstorff, P.; Addeo, F. Identification of N-linked glycoproteins in human milk by hydrophilic interaction liquid chromatography and mass spectrometry. Proteomics 2008, 8, 3833-3847
21. D'Alessandro, A.; Scaloni, A.; Zolla, L. Human milk proteins: An interactomics and updated functional overview. J. Proteome Res. 2010, 9, 3339-3373
22. Hettinga, K.; van Valenberg, H.; de Vries, S.; Boeren, S.; van Hooijdonk, T.; van Arendonk, J.; Vervoort, J. The host defense proteome of human and bovine milk. PLoS One 2011, 6, e19433
23. Liao, Y.; Alvarado, R.; Phinney, B.; Lonnerdal, B. Proteomic characterization of human milk fat globule membrane proteins during a 12 month lactation period. J. Proteome Res. 2011, 10, 3530-3541
24. Liao, Y.; Alvarado, R.; Phinney, B.; Lonnerdal, B. Proteomic characterization of human milk whey proteins during a twelve-month lactation period. J. Proteome Res. 2011, 10, 1746-1754
25. Lu, J.; Boeren, S.; de Vries, S.C.; van Valenberg, H.J.; Vervoort, J.; Hettinga, K. Filter-aided sample preparation with dimethyl labeling to identify and quantify milk fat globule membrane proteins. J. Proteomics 2011, 75, 34-43
26. Gao, X.; McMahon, R.J.; Woo, J.G.; Davidson, B.S.; Morrow, A.L.; Zhang, Q. Temporal changes in milk proteomes reveal developing milk functions. J. Proteome Res. 2012, 11, 3897-3907
27. Goldman, A.S.; Garza, C.; Nichols, B.L.; Goldblum, R.M. Immunologic factors in human milk during the first year of lactation. J. Pediatr. 1982, 100, 563-567
28. Keller, A.; Nesvizhskii, A.I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74, 5383-5392
29. Nesvizhskii, A.I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75, 4646-4658
30. Huang, D.W.; Sherman, B.T.; Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4, 44-57
31. Huang, D.W.; Sherman, B.T.; Lempicki, R.A. Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37, 1-13
32. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Statist. Soc. B 1995, 57, 289-300
33. Szklarczyk, D.; Franceschini, A.; Kuhn, M.; Simonovic, M.; Roth, A.; Minguez, P.; Doerks, T.; Stark, M.; Muller, J.; Bork, P.; et al. The STRING database in 2011: Functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 2011, 39, D561-D568
34. Alpert, A.J. Electrostatic repulsion hydrophilic interaction chromatography for isocratic separation of charged solutes and selective isolation of phosphopeptides. Anal. Chem. 2008, 80, 62-76
35. Hao, P.; Qian, J.; Ren, Y.; Sze, S.K. Electrostatic repulsion-hydrophilic interaction chromatography (ERLIC) versus strong cation exchange (SCX) for fractionation of iTRAQ-labeled peptides. J. Proteome Res. 2011, 10, 5568-5574
36. Hao, P.; Guo, T.; Li, X.; Adav, S.S.; Yang, J.; Wei, M.; Sze, S.K. Novel application of electrostatic repulsion-hydrophilic interaction chromatography (ERLIC) in shotgun proteomics: Comprehensive profiling of rat kidney proteome. J. Proteome Res. 2010, 9, 3520-3526
37. De Jong, E.P.; Griffin, T.J. Online nanoscale ERLIC-MS outperforms RPLC-MS for shotgun proteomics in complex mixtures. J. Proteome Res. 2012, 11, 5059-5064
38. Le, A.; Barton, L.D.; Sanders, J.T.; Zhang, Q. Exploration of bovine milk proteome in colostral and mature whey using an ion-exchange approach. J. Proteome Res. 2011, 10, 692-704
39. Emken, E.A.; Adlof, R.O.; Hachey, D.L.; Garza, C.; Thomas, M.R.; Brown-Booth, L. Incorporation of deuterium-labeled fatty acids into human milk, plasma, and lipoprotein phospholipids and cholesteryl esters. J. Lipid Res. 1989, 30, 395-402
40. Olofsson, S.O.; Boström, P.; Lagerstedt, J.; Andersson, L.; Adiels, M.; Perman, J.; Rutberg, M.; Li, L.; Borén, J. The lipid droplet: A dynamic organelle, not only involved in the storage and turnover of lipids. In Cellular Lipid Metabolism; Ehnholm, C., Ed.; Springer: New York, NY, USA, 2009; pp. 1-26
41. Doege, H.; Stahl, A. Protein-mediated fatty acid uptake: Novel insights from in vivo models. Physiology (Bethesda) 2006, 21, 259-268
42. Huuskonen, J.; Olkkonen, V.M.; Jauhiainen, M.; Ehnholm, C. The impact of phospholipid transfer protein (PLTP) on HDL metabolism. Atherosclerosis 2001, 155, 269-281
43. Heeren, J.; Beisiegel, U. Receptor-mediated endocytosis and intracellular trafficking of lipoproteins. In Cellular Lipid Metabolism; Ehnholm, C., Ed.; Springer: New York, NY, USA, 2009; pp. 213-235
44. Kersten, S. Angiopoietin-like proteins and lipid metabolism. In Cellular Lipid Metabolism; Ehnholm, C., Ed.; Springer: New York, NY, USA, 2009; pp. 237-249
45. Hachey, D.L.; Silber, G.H.; Wong, W.W.; Garza, C. Human lactation. II: Endogenous fatty acid synthesis by the mammary gland. Pediatr. Res. 1989, 25, 63-68
46. Cases, S.; Novak, S.; Zheng, Y.W.; Myers, H.M.; Lear, S.R.; Sande, E.; Welch, C.B.; Lusis, A.J.; Spencer, T.A.; Krause, B.R.; et al. ACAT-2, a second mammalian acyl-CoA: Cholesterol acyltransferase. Its cloning, expression, and characterization. J. Biol. Chem. 1998, 273, 26755-26764
47. Wustner, D.; Herrmann, A.; Hao, M.; Maxfield, F.R. Rapid nonvesicular transport of sterol between the plasma membrane domains of polarized hepatic cells. J. Biol. Chem. 2002, 277, 30325-30336
48. Prinz, W.A. Lipid trafficking sans vesicles: Where, why, how? Cell 2010, 143, 870-874
49. Robenek, H.; Hofnagel, O.; Buers, I.; Lorkowski, S.; Schnoor, M.; Robenek, M.J.; Heid, H.; Troyer, D.; Severs, N.J. Butyrophilin controls milk fat globule secretion. Proc. Natl. Acad. Sci. USA 2006, 103, 10385-10390
50. Rojas, R.; Apodaca, G. Immunoglobulin transport across polarized epithelial cells. Nat. Rev. Mol. Cell Biol. 2002, 3, 944-955
51. Jones, D.P. Redox potential of GSH/GSSG couple: Assay and biological significance. Methods Enzymol. 2002, 348, 93-112
52. West, M.B.; Segu, Z.M.; Feasley, C.L.; Kang, P.; Klouckova, I.; Li, C.; Novotny, M.V.; West, C.M.; Mechref, Y.; Hanigan, M.H. Analysis of site-specific glycosylation of renal and hepatic gamma-glutamyl transpeptidase from normal human tissue. J. Biol. Chem. 2010, 285, 29511-29524
53. Inoue, Y.; Kimura, A. Methylglyoxal and regulation of its metabolism in microorganisms. Adv. Microb. Physiol. 1995, 37, 177-227
54. Van Herwaarden, A.E.; Wagenaar, E.; Merino, G.; Jonker, J.W.; Rosing, H.; Beijnen, J.H.; Schinkel, A.H. Multidrug transporter ABCG2/breast cancer resistance protein secretes riboflavin (vitamin B2) into milk. Mol. Cell. Biol. 2007, 27, 1247-1253
55. Bosch, T.M.; Kjellberg, L.M.; Bouwers, A.; Koeleman, B.P.; Schellens, J.H.; Beijnen, J.H.; Smits, P.H.; Meijerman, I. Detection of single nucleotide polymorphisms in the ABCG2 gene in a Dutch population. Am. J. Pharmacogenomics 2005, 5, 123-131
56. Vlaming, M.L.; Lagas, J.S.; Schinkel, A.H. Physiological and pharmacological roles of ABCG2 (BCRP): Recent findings in Abcg2 knockout mice. Adv. Drug Deliv. Rev. 2009, 61, 14-25
57. Field, C.J. The immunological components of human milk and their effect on immune development in infants. J. Nutr. 2005, 135, 1-4
58. Murphy, K.P. Janeway's Immunobiology, 8th ed.; Garland Science: London, UK, 2012; pp. 48-71, 527-528
59. Hachey, D.L.; Thomas, M.R.; Emken, E.A.; Garza, C.; Brown-Booth, L.; Adlof, R.O.; Klein, P.D. Human lactation: Maternal transfer of dietary triglycerides labeled with stable isotopes. J. Lipid Res. 1987, 28, 1185-1192
60. Insull, W., Jr.; Hirsch, J.; James, T.; Ahrens, E.H., Jr. The fatty acids of human milk. II. Alterations produced by manipulation of caloric balance and exchange of dietary fats. J. Clin. Invest. 1959, 38, 443-450
61. Neville, M.C.; Picciano, M.F. Regulation of milk lipid secretion and composition. Annu. Rev. Nutr. 1997, 17, 159-183
62. Kay, J.K.; Weber, W.J.; Moore, C.E.; Bauman, D.E.; Hansen, L.B.; Chester-Jones, H.; Crooker, B.A.; Baumgard, L.H. Effects of week of lactation and genetic selection for milk yield on milk fatty acid composition in Holstein cows. J. Dairy Sci. 2005, 88, 3886-3893
63. Shingfield, K.J.; Bernard, L.; Leroux, C.; Chilliard, Y. Role of trans fatty acids in the nutritional regulation of mammary lipogenesis in ruminants. Animal 2010, 4, 1140-1166
64. Mach, N.; van Baal, J.; Kruijt, L.; Jacobs, A.; Smits, M. Dietary unsaturated fatty acids affect the mammary gland integrity and health in lactating dairy cows. BMC Proc. 2011, 5, doi:10.1186/1753-6561-5-S4-S35
65. Chaturvedi, P.; Warren, C.D.; Altaye, M.; Morrow, A.L.; Ruiz-Palacios, G.; Pickering, L.K.; Newburg, D.S. Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology 2001, 11, 365-372
66. Carlson, S.E. N-Acetylneuraminic acid concentrations in human milk oligosaccharides and glycoproteins during lactation. Am. J. Clin. Nutr. 1985, 41, 720-726
67. Chichlowski, M.; German, J.B.; Lebrilla, C.B.; Mills, D.A. The influence of milk oligosaccharides on microbiota of infants: Opportunities for formulas. Annu. Rev. Food Sci. Technol. 2011, 2, 331-351
68. Newburg, D.S.; Ruiz-Palacios, G.M.; Morrow, A.L. Human milk glycans protect infants against enteric pathogens. Annu. Rev. Nutr. 2005, 25, 37-58
69. Page, M.J.; Amess, B.; Townsend, R.R.; Parekh, R.; Herath, A.; Brusten, L.; Zvelebil, M.J.; Stein, R.C.; Waterfield, M.D.; Davies, S.C.; et al. Proteomic definition of normal human luminal and myoepithelial breast cells purified from reduction mammoplasties. Proc. Natl. Acad. Sci. USA 1999, 96, 12589-12594
70. Jacobs, J.M.; Mottaz, H.M.; Yu, L.R.; Anderson, D.J.; Moore, R.J.; Chen, W.N.; Auberry, K.J.; Strittmatter, E.F.; Monroe, M.E.; Thrall, B.D.; et al. Multidimensional proteome analysis of human mammary epithelial cells. J. Proteome Res. 2004, 3, 68-75
71. Jacobs, J.M.; Waters, K.M.; Kathmann, L.E.; Camp, D.G., 2nd; Wiley, H.S.; Smith, R.D.; Thrall, B.D. The mammary epithelial cell secretome and its regulation by signal transduction pathways. J. Proteome Res. 2008, 7, 558-569