Advertisement

Proteomics in Milk and Milk Processing

Chapter
Part of the Food Microbiology and Food Safety book series (FMFS, volume 2)

Abstract

Milk proteins provide essential nutrition for growth and represent an expansive repertoire of functional food ingredients. Many proteins are thoroughly digested in the gut to provide vital amino acids, however, others are only partially or minimally broken down and thus able to exert higher-level functionality related to the structures of their digestive products. Defining the milk proteome and how it changes during the course of lactation are key steps towards an improved understanding of milk biology and function, and has the potential to provide novel insights in the areas of dairy and other food sciences. This better understanding may also guide manufacturers in developing foods with improved protein quality and function. Recent progress in proteomics has greatly increased the number of proteins identified in milk. In this chapter, we highlight recent findings in both human and bovine milk proteomes that are novel or whose importance is not yet fully understood. We describe the consequences of these findings on our understanding of the role of milk proteins in biological processes, signaling pathways, and nutrition, and as functional food ingredients. We further describe the use of proteomics in characterizing heat-induced protein modifications during industrial processes that often reduce the nutritional value and function of milk proteins. Finally, we discuss the use of proteomic analysis as a guide in the optimization of industrial processing conditions and selection of milk materials.

Keywords

Human Milk Whey Protein Milk Protein Casein Micelle Early Lactation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abbott RD, Curb JD, Rodriguez BL, Sharp DS, Burchfiel CM, Yano K (1996) Effect of dietary calcium and milk consumption on risk of thromboembolic stroke in older middle-aged men. The Honolulu Heart Program. Stroke 27(5):813–818CrossRefGoogle Scholar
  2. Acharya AS, Manning JM (1980) Amadori rearrangement of glyceraldehyde-hemoglobin Schiff base adducts. A new procedure for the determination of ketoamine adducts in proteins. J Biol Chem 255(15):7218–7224Google Scholar
  3. Affolter M, Grass L, Vanrobaeys F, Casado B, Kussmann M (2009) Qualitative and quantitative profiling of the bovine milk fat globule membrane proteome. J Proteomics 73(6):1079–1088CrossRefGoogle Scholar
  4. Arena S, Renzone G, Novi G, Paffetti A, Bernardini G, Santucci A, Scaloni A (2010) Modern proteomic methodologies for the characterization of lactosylation protein targets in milk. Proteomics 10(19):3414–3434CrossRefGoogle Scholar
  5. Belford DA, Rogers ML, Regester GO, Francis GL, Smithers GW, Liepe IJ, Priebe IK, Ballard FJ (1995) Milk-derived growth factors as serum supplements for the growth of fibroblast and epithelial cells. In Vitro Cell Dev Biol Anim 31(10):752–760CrossRefGoogle Scholar
  6. Bottcher MF, Jenmalm MC, Garofalo RP, Bjorksten B (2000a) Cytokines in breast milk from allergic and nonallergic mothers. Pediatr Res 47(1):157–162CrossRefGoogle Scholar
  7. Bottcher MF, Jenmalm MC, Bjorksten B, Garofalo RP (2000b) Chemoattractant factors in breast milk from allergic and nonallergic mothers. Pediatr Res 47(5):592–597CrossRefGoogle Scholar
  8. Bottcher MF, Jenmalm MC, Bjorksten B (2003) Cytokine, chemokine and secretory IgA levels in human milk in relation to atopic disease and IgA production in infants. Pediatr Allergy Immunol 14(1):35–41CrossRefGoogle Scholar
  9. Bryan DL, Forsyth KD, Gibson RA, Hawkes JS (2006) Interleukin-2 in human milk: a potential modulator of lymphocyte development in the breastfed infant. Cytokine 33(5):289–293CrossRefGoogle Scholar
  10. Calhoun DA, Lunoe M, Du Y, Staba SL, Christensen RD (1999) Concentrations of granulocyte colony-stimulating factor in human milk after in vitro simulations of digestion. Pediatr Res 46(6):767–771CrossRefGoogle Scholar
  11. Carbonaro M (2004) Proteomics: present and future in food quality evaluation. Trends Food Sci Tech 15:209–216CrossRefGoogle Scholar
  12. Carbonaro M (2006) Application of two-dimensional electrophoresis for monitoring gastrointestinal digestion of milk. Amino Acids 31(4):485–488CrossRefGoogle Scholar
  13. Casado B, Affolter M, Kussmann M (2009) OMICS-rooted studies of milk proteins, oligosaccharides and lipids. J Proteomics 73(2):196–208CrossRefGoogle Scholar
  14. Castell JV, Friedrich G, Kuhn CS, Poppe GE (1997) Intestinal absorption of undegraded proteins in men: presence of bromelain in plasma after oral intake. Am J Physiol Gastr L 273((1 36–1)):G139–G146Google Scholar
  15. Cattaneo S, Masotti F, Pellegrino L (2009) Liquid infant formulas: technological tools for limiting heat damage. J Agric Food Chem 57(22):10689–10694CrossRefGoogle Scholar
  16. Cavaletto M, Giuffrida MG, Conti A (2004) The proteomic approach to analysis of human milk fat globule membrane. Clin Chim Acta 347(1–2):41–48CrossRefGoogle Scholar
  17. Cavaletto M, Giuffrida MG, Conti A (2008) Milk fat globule membrane components–a proteomic approach. Adv Exp Med Biol 606:129–141CrossRefGoogle Scholar
  18. Cebo C, Caillat H, Bouvier F, Martin P (2010) Major proteins of the goat milk fat globule membrane. J Dairy Sci 93(3):868–876CrossRefGoogle Scholar
  19. Cebo C, Rebours E, Henry C, Makhzami S, Cosette P, Martin P (2012) Identification of major milk fat globule membrane proteins from pony mare milk highlights the molecular diversity of lactadherin across species. J Dairy Sci 95(3):1085–1098CrossRefGoogle Scholar
  20. Charlwood J, Hanrahan S, Tyldesley R, Langridge J, Dwek M, Camilleri P (2002) Use of proteomic methodology for the characterization of human milk fat globular membrane proteins. Anal Biochem 301(2):314–324CrossRefGoogle Scholar
  21. Chevalier F, Hirtz C, Sommerer N, Kelly AL (2009) Use of reducing/nonreducing two-dimensional electrophoresis for the study of disulfide-mediated interactions between proteins in raw and heated bovine milk. J Agric Food Chem 57(13):5948–5955CrossRefGoogle Scholar
  22. Clare DA, Swaisgood HE (2000) Bioactive milk peptides: a prospectus. J Dairy Sci 83(6):1187–1195CrossRefGoogle Scholar
  23. Clare DA, Catignani GL, Swaisgood HE (2003) Biodefense properties of milk: the role of antimicrobial proteins and peptides. Curr Pharm Design 9(16):1239–1255CrossRefGoogle Scholar
  24. Cunsolo V, Muccilli V, Saletti R, Foti S (2011a) Review: applications of mass spectrometry techniques in the investigation of milk proteome. Eur J Mass Spectrom (Chichester, Eng) 17(4):305–320CrossRefGoogle Scholar
  25. Cunsolo V, Muccilli V, Fasoli E, Saletti R, Righetti PG, Foti S (2011b) Poppea’s bath liquor: the secret proteome of she-donkey’s milk. J Proteomics 74(10):2083–2099CrossRefGoogle Scholar
  26. Czerwenka C, Maier I, Pittner F, Lindner W (2006) Investigation of the lactosylation of whey proteins by liquid chromatography-mass spectrometry. J Agric Food Chem 54(23):8874–8882CrossRefGoogle Scholar
  27. D’Alessandro A, Scaloni A, Zolla L (2010) Human milk proteins: an interactomics and updated functional overview. J Proteome Res 9(7):3339–3373CrossRefGoogle Scholar
  28. 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. J Proteome Res 8(8):3925–3936CrossRefGoogle Scholar
  29. Daniels MC, Adair LS (2005) Breast-feeding influences cognitive development in Filipino children. J Nutr 135(11):2589–2595Google Scholar
  30. De Matteis MA, Luini A (2008) Exiting the golgi complex. Nat Rev Mol Cell Biol 9(4):273–284CrossRefGoogle Scholar
  31. Desrivieres S, Prinz T, Castro-Palomino Laria N, Meyer M, Boehm G, Bauer U, Schafer J, Neumann T, Shemanko C, Groner B (2003) Comparative proteomic analysis of proliferating and functionally differentiated mammary epithelial cells. Mol Cell Proteomics 2(10):1039–1054CrossRefGoogle Scholar
  32. Dewettinck K, Rombaut R, Thienpont N, Le TT, Messens K, Van Camp J (2008) Nutritional and technological aspects of milk fat globule membrane material. Int Dairy J 18(5):436–457CrossRefGoogle Scholar
  33. Donnet-Hughes A, Duc N, Serrant P, Vidal K, Schiffrin EJ (2000) Bioactive molecules in milk and their role in health and disease: the role of transforming growth factor-beta. Immunol Cell Biol 78(1):74–79CrossRefGoogle Scholar
  34. Fenaille F, Morgan F, Parisod V, Tabet JC, Guy PA (2004) Solid-state glycation of beta-lactoglobulin by lactose and galactose: localization of the modified amino acids using mass spectrometric techniques. J Mass Spectrom 39(1):16–28CrossRefGoogle Scholar
  35. Field CJ (2005) The immunological components of human milk and their effect on immune development in infants. J Nutr 135(1):1–4Google Scholar
  36. Fong BY, Norris CS, MacGibbon AKH (2007) Protein and lipid composition of bovine milk-fat-globule membrane. Int Dairy J 17(4):275–288CrossRefGoogle Scholar
  37. Fortunato D, Giuffrida MG, Cavaletto M, Garoffo LP, Dellavalle G, Napolitano L, Giunta C, Fabris C, Bertino E, Coscia A, Conti A (2003) Structural proteome of human colostral fat globule membrane proteins. Proteomics 3(6):897–905CrossRefGoogle Scholar
  38. Frid AH, Nilsson M, Holst JJ, Bjorck IM (2005) Effect of whey on blood glucose and insulin responses to composite breakfast and lunch meals in type 2 diabetic subjects. Am J Clin Nutr 82(1):69–75Google Scholar
  39. Gao X, McMahon RJ, Woo JG, Davidson BS, Morrow AL, Zhang Q (2012) Temporal changes in milk proteomes reveal developing milk functions. J Proteome Res 11:3897–3907CrossRefGoogle Scholar
  40. German JB, Dillard CJ, Ward RE (2002) Bioactive components in milk. Curr Opin Clin Nutr 5(6):653–658CrossRefGoogle Scholar
  41. Gill HS, Cross ML (2000) Anticancer properties of bovine milk. Br J Nutr 84(Suppl 1):S161–S166Google Scholar
  42. Gobbetti M, Stepaniak L, De Angelis M, Corsetti A, Di Cagno R (2002) Latent bioactive peptides in milk proteins: proteolytic activation and significance in dairy processing. Crit Rev Food Sci 42(3):223–239CrossRefGoogle Scholar
  43. Goldman AS (1993) The immune system of human milk: antimicrobial, antiinflammatory and immunomodulating properties. Pediatr Infect Dis J 12(8):664–671CrossRefGoogle Scholar
  44. Hamosh M (2001) Bioactive factors in human milk. Pediatr Clin North Am 48(1):69–86CrossRefGoogle Scholar
  45. Hanash SM, Pitteri SJ, Faca VM (2008) Mining the plasma proteome for cancer biomarkers. Nature 452(7187):571–579CrossRefGoogle Scholar
  46. Hanson LA, Korotkova M, Lundin S, Haversen L, Silfverdal SA, Mattsby-Baltzer I, Strandvik B, Telemo E (2003) The transfer of immunity from mother to child. Ann N Y Acad Sci 987:199–206CrossRefGoogle Scholar
  47. Harmsen HJM, Wildeboer-Veloo ACM, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, Welling GW (2000) Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30(1):61–67CrossRefGoogle Scholar
  48. Harris P, Johannessen KM, Smolenski G, Callaghan M, Broadhurst MK, Kim K, Wheeler TT (2010) Characterisation of the anti-microbial activity of bovine milk ribonuclease4 and ribonuclease5 (angiogenin). Int Dairy J 20(6):400–407CrossRefGoogle Scholar
  49. Hawkes JS, Bryan DL, Neumann MA, Makrides M, Gibson RA (2001) Transforming growth factor beta in human milk does not change in response to modest intakes of docosahexaenoic acid. Lipids 36(10):1179–1181CrossRefGoogle Scholar
  50. Heid HW, Keenan TW (2005) Intracellular origin and secretion of milk fat globules. Eur J Cell Biol 84(2–3):245–258CrossRefGoogle Scholar
  51. Heird WC, Schwarz SM, Hansen IH (1984) Colostrum-induced enteric mucosal growth in beagle puppies. Pediatr Res 18(6):512–515CrossRefGoogle Scholar
  52. Hering NA, Andres S, Fromm A, van Tol EA, Amasheh M, Mankertz J, Fromm M, Schulzke JD (2011) Transforming growth factor-beta, a whey protein component, strengthens the intestinal barrier by upregulating claudin-4 in HT-29/B6 cells. J Nutr 141(5):783–789CrossRefGoogle Scholar
  53. 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):e19433CrossRefGoogle Scholar
  54. Holland JW, Gupta R, Deeth HC, Alewood PF (2011) Proteomic analysis of temperature-dependent changes in stored UHT milk. J Agric Food Chem 59(5):1837–1846CrossRefGoogle Scholar
  55. Hong SS, Park JH, Kwon SW (2007) Determination of proteins in infant formula by high-performance liquid chromatography-electrospray tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 845(1):69–73CrossRefGoogle Scholar
  56. Huang DW, Sherman BT, Lempicki RA (2009a) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57CrossRefGoogle Scholar
  57. Huang DW, Sherman BT, Lempicki RA (2009b) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37(1):1–13CrossRefGoogle Scholar
  58. Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326(5957):1216–1219CrossRefGoogle Scholar
  59. Jenness R (1979) The composition of human milk. Semin Perinatol 3(3):225–239Google Scholar
  60. Jones AD, Tier CM, Wilkins JP (1998) Analysis of the Maillard reaction products of beta-lactoglobulin and lactose in skimmed milk powder by capillary electrophoresis and electrospray mass spectrometry. J Chromatogr A 822(1):147–154CrossRefGoogle Scholar
  61. Kanwar JR, Kanwar RK (2009) Gut health immunomodulatory and anti-inflammatory functions of gut enzyme digested high protein micro-nutrient dietary supplement-Enprocal. BMC Immunol 10(7):1–19Google Scholar
  62. Karhumaa P, Leinonen J, Parkkila S, Kaunisto K, Tapanainen J, Rajaniemi H (2001) The identification of secreted carbonic anhydrase VI as a constitutive glycoprotein of human and rat milk. Proc Natl Acad Sci USA 98(20):11604–11608CrossRefGoogle Scholar
  63. Keenan TW (2001) Milk lipid globules and their surrounding membrane: a brief history and perspectives for future research. J Mammary Gland Biol Neoplasia 6(3):365–371CrossRefGoogle Scholar
  64. Knip M, Virtanen SM, Seppa K, Ilonen J, Savilahti E, Vaarala O, Reunanen A, Teramo K, Hamalainen AM, Paronen J, Dosch HM, Hakulinen T, Akerblom HK (2010) Dietary intervention in infancy and later signs of beta-cell autoimmunity. N Engl J Med 363(20):1900–1908CrossRefGoogle Scholar
  65. Korhonen H, Pihlanto A (2003) Food-derived bioactive peptides–opportunities for designing future foods. Curr Pharm Design 9(16):1297–1308CrossRefGoogle Scholar
  66. Korhonen H, Pihlanto A (2007) Technological options for the production of health-promoting proteins and peptides derived from milk and colostrum. Curr Pharm Design 13(8):829–843CrossRefGoogle Scholar
  67. Kunz C, Lonnerdal B (1992) Re-evaluation of the whey protein/casein ratio of human milk. Acta Paediatr 81(2):107–112CrossRefGoogle Scholar
  68. Le A, Barton LD, Sanders JT, Zhang Q (2011) Exploration of bovine milk proteome in colostral and mature whey using an ion-exchange approach. J Proteome Res 10(2):692–704CrossRefGoogle Scholar
  69. Le TT, Deeth HC, Bhandari B, Alewood PF, Holland JW (2012) A proteomic approach to detect lactosylation and other chemical changes in stored milk protein concentrate. Food Chem 132:655–662CrossRefGoogle Scholar
  70. Leonil J, Molle D, Fauquant J, Maubois JL, Pearce RJ, Bouhallab S (1997) Characterization by ionization mass spectrometry of lactosyl beta-lactoglobulin conjugates formed during heat treatment of milk and whey and identification of one lactose-binding site. J Dairy Sci 80(10):2270–2281CrossRefGoogle Scholar
  71. Liao Y, Alvarado R, Phinney B, Lonnerdal B (2011a) Proteomic characterization of human milk fat globule membrane proteins during a 12 month lactation period. J Proteome Res 10(8):3530–3541CrossRefGoogle Scholar
  72. Liao Y, Alvarado R, Phinney B, Lonnerdal B (2011b) Proteomic characterization of human milk whey proteins during a twelve-month lactation period. J Proteome Res 10(4):1746–1754CrossRefGoogle Scholar
  73. Lönnerdal B (2003) Nutritional and physiologic significance of human milk proteins. Am J Clin Nutr 77(6):1535s–1536sGoogle Scholar
  74. Lönnerdal B (2004) Human milk proteins: key components for the biological activity of human milk. Adv Exp Med Biol 554:11–25Google Scholar
  75. Losito I, Carbonara T, Monaci L, Palmisano F (2007) Evaluation of the thermal history of bovine milk from the lactosylation of whey proteins: an investigation by liquid chromatography-electrospray ionization mass spectrometry. Anal Bioanal Chem 389(7–8):2065–2074CrossRefGoogle Scholar
  76. Lu J, Boeren S, de Vries SC, van Valenberg HJ, Vervoort J, Hettinga K (2011) Filter-aided sample preparation with dimethyl labeling to identify and quantify milk fat globule membrane proteins. J Proteomics 75(1):34–43CrossRefGoogle Scholar
  77. Luhovyy BL, Akhavan T, Anderson GH (2007) Whey proteins in the regulation of food intake and satiety. J Am Coll Nutr 26(6):704S–712SGoogle Scholar
  78. Luz Sanz M, Corzo-Martinez M, Rastall RA, Olano A, Moreno FJ (2007) Characterization and in vitro digestibility of bovine beta-lactoglobulin glycated with galactooligosaccharides. J Agric Food Chem 55(19):7916–7925CrossRefGoogle Scholar
  79. Mahe S, Roos N, Benamouzig R, Davin L, Luengo C, Gagnon L, Gausserges N, Rautureau J, Tome D (1996) Gastrojejunal kinetics and the digestion of [15N]beta-lactoglobulin and casein in humans: the influence of the nature and quantity of the protein. Am J Clin Nutr 63(4):546–552Google Scholar
  80. Mangé A, Bellet V, Tuaillon E, Van de Perre P, Solassol J (2008) Comprehensive proteomic analysis of the human milk proteome: contribution of protein fractionation. J Chromatogr B 876(2):252–256CrossRefGoogle Scholar
  81. Mauron J (1990) Influence of processing on protein quality. J Nutr Sci Vitaminol (Tokyo) 36(Suppl 1):S57–S69CrossRefGoogle Scholar
  82. Meltretter J, Pischetsrieder M (2008) Application of mass spectrometry for the detection of glycation and oxidation products in milk proteins. Ann N Y Acad Sci 1126:134–140CrossRefGoogle Scholar
  83. Meltretter J, Seeber S, Humeny A, Becker CM, Pischetsrieder M (2007) Site-specific formation of Maillard, oxidation, and condensation products from whey proteins during reaction with lactose. J Agric Food Chem 55(15):6096–6103CrossRefGoogle Scholar
  84. Meltretter J, Birlouez-Aragon I, Becker CM, Pischetsrieder M (2009) Assessment of heat treatment of dairy products by MALDI-TOF-MS. Mol Nutr Food Res 53(12):1487–1495CrossRefGoogle Scholar
  85. Mesmin C, Fenaille F, Becher F, Tabet JC, Ezan E (2011) Identification and characterization of apelin peptides in bovine colostrum and milk by liquid chromatography-mass spectrometry. J Proteome Res 10(11):5222–5231CrossRefGoogle Scholar
  86. Monaci L, van Hengel AJ (2007) Effect of heat treatment on the detection of intact bovine beta-lactoglobulins by LC mass spectrometry. J Agric Food Chem 55(8):2985–2992CrossRefGoogle Scholar
  87. Morgan F, Leonil J, Molle D, Bouhallab S (1997) Nonenzymatic lactosylation of bovine beta-lactoglobulin under mild heat treatment leads to structural heterogeneity of the glycoforms. Biochem Biophys Res Commun 236(2):413–417CrossRefGoogle Scholar
  88. Morrison B, Cutler ML (2010) The contribution of adhesion signaling to lactogenesis. J Cell Commun Signal 4(3):131–139CrossRefGoogle Scholar
  89. Murphy KP (2012) Janeway’s immunobiology, 8th edn. Garland Science, London, pp 48–71, 527–528Google Scholar
  90. Nagpal R, Behare P, Rana R, Kumar A, Kumar M, Arora S, Morotta F, Jain S, Yadav H (2011) Bioactive peptides derived from milk proteins and their health beneficial potentials: an update. Food Funct 2(1):18–27CrossRefGoogle Scholar
  91. Ogundele MO (2001) Role and significance of the complement system in mucosal immunity: particular reference to the human breast milk complement. Immunol Cell Biol 79(1):1–10CrossRefGoogle Scholar
  92. Pal S, Ellis V (2010) The chronic effects of whey proteins on blood pressure, vascular function, and inflammatory markers in overweight individuals. Obesity (Silver Spring) 18(7):1354–1359CrossRefGoogle Scholar
  93. Pal S, Ellis V (2011) Acute effects of whey protein isolate on blood pressure, vascular function and inflammatory markers in overweight postmenopausal women. Br J Nutr 105(10):1512–1519CrossRefGoogle Scholar
  94. Palmer DJ, Kelly VC, Smit AM, Kuy S, Knight CG, Cooper GJ (2006) Human colostrum: identification of minor proteins in the aqueous phase by proteomics. Proteomics 6(7):2208–2216CrossRefGoogle Scholar
  95. Peterson JA, Scallan CD, Ceriani RL, Hamosh M (2001) Structural and functional aspects of three major glycoproteins of the human milk fat globule membrane. Adv Exp Med Biol 501:179–187CrossRefGoogle Scholar
  96. Pihlanto A, Korhonen H (2003) Bioactive peptides and proteins. Adv Food Nutr Res 47:175–276CrossRefGoogle Scholar
  97. Pisanu S, Ghisaura S, Pagnozzi D, Biosa G, Tanca A, Roggio T, Uzzau S, Addis MF (2011) The sheep milk fat globule membrane proteome. J Proteomics 74(3):350–358CrossRefGoogle Scholar
  98. Reinhardt TA, Lippolis JD (2006) Bovine milk fat globule membrane proteome. J Dairy Res 73(4):406–416CrossRefGoogle Scholar
  99. Reinhardt TA, Lippolis JD (2008) Developmental changes in the milk fat globule membrane proteome during the transition from colostrum to milk. J Dairy Sci 91(6):2307–2318CrossRefGoogle Scholar
  100. Ricci-Cabello I, Herrera MO, Artacho R (2012) Possible role of milk-derived bioactive peptides in the treatment and prevention of metabolic syndrome. Nutr Rev 70(4):241–255CrossRefGoogle Scholar
  101. Riccio P (2004) The proteins of the milk fat globule membrane in the balance. Trends Food Sci Tech 15(9):458–461CrossRefGoogle Scholar
  102. Rojas R, Apodaca G (2002) Immunoglobulin transport across polarized epithelial cells. Nat Rev Mol Cell Biol 3(12):944–955CrossRefGoogle Scholar
  103. Roos N, Mahe S, Benamouzig R, Sick H, Rautureau J, Tome D (1995) 15N-labeled immunoglobulins from bovine colostrum are partially resistant to digestion in human intestine. J Nutr 125(5):1238–1244Google Scholar
  104. Sanderson IR, Walker WA (2000) Development of the gastrointestinal tract. B. C. Decker, Hamilton, Ontario L8N 3K7, pp 83–102, 147–164, 227–260Google Scholar
  105. Satake M, Enjoh M, Nakamura Y, Takano T, Kawamura Y, Arai S, Shimizu M (2002) Transepithelial transport of the bioactive tripeptide, Val-Pro-Pro, in human intestinal Caco-2 cell monolayers. Biosci Biotechnol Biochem 66(2):378–384CrossRefGoogle Scholar
  106. Schack-Nielsen L, Michaelsen KF (2007) Advances in our understanding of the biology of human milk and its effects on the offspring. J Nutr 137(2):503S–510SGoogle Scholar
  107. Schlimme E, Meisel H (1995) Bioactive peptides derived from milk proteins. Structural, physiological and analytical aspects. Nahrung 39(1):1–20CrossRefGoogle Scholar
  108. Seiquer I, Diaz-Alguacil J, Delgado-Andrade C, Lopez-Frias M, Munoz Hoyos A, Galdo G, Navarro MP (2006) Diets rich in Maillard reaction products affect protein digestibility in adolescent males aged 11–14 y. Am J Clin Nutr 83(5):1082–1088Google Scholar
  109. Séverin S, Wenshui X (2005) Milk biologically active components as nutraceuticals: review. Crit Rev Food Sci 45(7–8):645–656CrossRefGoogle Scholar
  110. Shimizu M, Tsunogai M, Arai S (1997) Transepithelial transport of oligopeptides in the human intestinal cell, Caco-2. Peptides 18(5):681–687CrossRefGoogle Scholar
  111. Siciliano R, Rega B, Amoresano A, Pucci P (2000) Modern mass spectrometric methodologies in monitoring milk quality. Anal Chem 72(2):408–415CrossRefGoogle Scholar
  112. Smithers GW (2008) Whey and whey proteins-from ‘gutter-to-gold’. Int Dairy J 18(7):695–704CrossRefGoogle Scholar
  113. 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. J Proteome Res 6(1):207–215CrossRefGoogle Scholar
  114. Sorva R, Makinen-Kiljunen S, Juntunen-Backman K (1994) β-Lactoglobulin secretion in human milk varies widely after cow’s milk ingestion in mothers of infants with cow’s milk allergy. J Allergy Clin Immunol 93(4):787–792CrossRefGoogle Scholar
  115. Spitsberg VL (2005) Invited review: bovine milk fat globule membrane as a potential nutraceutical. J Dairy Sci 88(7):2289–2294CrossRefGoogle Scholar
  116. van Boekel MAJS (1998) Effect of heating on Maillard reactions in milk. Food Chem 62(4):403–414CrossRefGoogle Scholar
  117. Vanderghem C, Blecker C, Danthine S, Deroanne C, Haubruge E, Guillonneau F, De Pauw E, Francis F (2008) Proteome analysis of the bovine milk fat globule: enhancement of membrane purification. Int Dairy J 18(9):885–893CrossRefGoogle Scholar
  118. Walker WA (2010) Mead Johnson Symposium: functional proteins in human milk: role in infant health and development. J Pediatr 156(2 Suppl):S1–S2Google Scholar
  119. Wiseman BS, Werb Z (2002) Stromal effects on mammary gland development and breast cancer. Science 296(5570):1046–1049CrossRefGoogle Scholar
  120. 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(16):3470–3482CrossRefGoogle Scholar
  121. Zhang Q, Faca V, Hanash S (2011) Mining the plasma proteome for disease applications across seven logs of protein abundance. J Proteome Res 10(1):46–50CrossRefGoogle Scholar
  122. Zivkovic AM, German JB, Lebrilla CB, Mills DA (2011) Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci USA 108(Suppl 1):4653–4658CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Mead Johnson Nutrition Pediatric Nutrition InstituteEvansvilleUSA
  2. 2.Department of Chemistry and BiochemistryUniversity of California-Santa BarbaraSanta BarbaraUSA

Personalised recommendations