Structures and metabolic properties of bovine milk oligosaccharides and their potential in the development of novel therapeutics

Frontiers in Nutrition

Volumn 6, Issue , 2019, Pages

  Robinson, Randall C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mass spectrometry; Milk; Obesity; Prebiotic; Therapeutic

Indexed keywords

EID: 85067787664     PISSN: None     EISSN: 2296861X     Source Type: Journal    
DOI: 10.3389/fnut.2019.00050     Document Type: Short Survey

References (77)

1. Bode, L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology. (2012) 22:1147–62. 10.1093/glycob/cws074, 22513036.
2. Morrow, AL, Newburg, DS. Human milk oligosaccharide. In: Neu, J, Poindexter, B, Polin, RA, editors. Gastroenterology and Nutrition: Neonatology Questions and Controversies. Philadelphia, PA: Elsevier (2019). p. 43–58.
3. Wu, S, Tao, N, German, JB, Grimm, R, Lebrilla, CB. Development of an annotated library of neutral human milk oligosaccharides. J Proteome Res. (2010) 9:4138–51. 10.1021/pr100362f, 20578730.
4. Ninonuevo, MR, Park, Y, Yin, H, Zhang, J, Ward, RE, Clowers, BH,. A strategy for annotating the human milk glycome. J Agric Food Chem. (2006) 54:7471–80. 10.1021/jf0615810, 17002410.
5. LoCascio, RG, Ninonuevo, MR, Freeman, SL, Sela, DA, Grimm, R, Lebrilla, CB,. Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J Agric Food Chem. (2007) 55:8914–9. 10.1021/jf0710480, 17915960.
6. Marcobal, A, Barboza, M, Froehlich, JW, Block, DE, German, JB, Lebrilla, CB,. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem. (2010) 58:5334–40. 10.1021/jf9044205, 20394371.
7. Yu, Z-T, Chen, C, Newburg, DS. Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes. Glycobiology. (2013) 23:1281–92. 10.1093/glycob/cwt065, 24013960.
8. Hardy, H, Harris, J, Lyon, E, Beal, J, Foey, AD. Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients. (2013) 5:1869–912. 10.3390/nu5061869, 23760057.
9. Aldredge, DL, Geronimo, MR, Hua, S, Nwosu, CC, Lebrilla, CB, Barile, D. Annotation and structural elucidation of bovine milk oligosaccharides and determination of novel fucosylated structures. Glycobiology. (2013) 23:664–76. 10.1093/glycob/cwt007, 23436288.
10. Gopal, PK, Gill, HS. Oligosaccharides and glycoconjugates in bovine milk and colostrum. Br J Nutr. (2000) 84:69–74. 10.1017/S0007114500002270, 11242449.
11. Kirmiz, N, Robinson, RC, Shah, IM, Barile, D, Mills, DA. Milk glycans and their interaction with the infant gut microbiota. Annu Rev Food Sci Technol. (2018) 9:429–50. 10.1146/annurev-food-030216-030207, 29580136.
12. Tao, N, DePeters, EJ, Freeman, S, German, JB, Grimm, R, Lebrilla, CB. Bovine milk glycome. J Dairy Sci. (2008) 91:3768–78. 10.3168/jds.2008-1305, 18832198.
13. Barile, D, Marotta, M, Chu, C, Mehra, R, Grimm, R, Lebrilla, CB,. Neutral and acidic oligosaccharides in Holstein-Friesian colostrum during the first 3 days of lactation measured by high performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry. J Dairy Sci. (2010) 93:3940–9. 10.3168/jds.2010-3156, 20723667.
14. Tao, N, DePeters, EJ, German, JB, Grimm, R, Lebrilla, CB. Variations in bovine milk oligosaccharides during early and middle lactation stages analyzed by high-performance liquid chromatography-chip/mass spectrometry. J Dairy Sci. (2009) 92:2991–3001. 10.3168/jds.2008-1642, 19528576.
15. Mehra, R, Barile, D, Marotta, M, Lebrilla, CB, Chu, C, German, JB. Novel high-molecular weight fucosylated milk oligosaccharides identified in dairy streams. PLoS ONE. (2014) 9:e96040. 10.1371/journal.pone.0096040, 24810963.
16. Sundekilde, UK, Barile, D, Meyrand, M, Poulsen, NA, Larsen, LB, Lebrilla, CB,. Natural variability in bovine milk oligosaccharides from Danish Jersey and Holstein-Friesian breeds. J Agric Food Chem. (2012) 60:6188–96. 10.1021/jf300015j, 22632419.
17. Ruiz-Palacios, GM, Cervantes, LE, Ramos, P, Chavez-Munguia, B, Newburg, DS. Campylobacter jejuni binds intestinal H (O) antigen (Fucα1, 2Galβ1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem. (2003) 278:14112–20. 10.1074/jbc.M207744200.
18. Fong, B, Ma, K, McJarrow, P. Quantification of bovine milk oligosaccharides using liquid chromatography–selected reaction monitoring–mass spectrometry. J Agric Food Chem. (2011) 59:9788–95. 10.1021/jf202035m, 21790206.
19. Kailemia, MJ, Ruhaak, LR, Lebrilla, CB, Amster, IJ. Oligosaccharide analysis by mass spectrometry: a review of recent developments. Anal Chem. (2014) 86:196–212. 10.1021/ac403969n, 24313268.
20. Wu, S, Grimm, R, German, JB, Lebrilla, CB. Annotation and structural analysis of sialylated human milk oligosaccharides. J Proteome Res. (2011) 10:856–68. 10.1021/pr101006u, 21133381.
21. Galermo, AG, Nandita, E, Barboza, M, Amicucci, MJ, Vo, T-TT, Lebrilla, CB. Liquid chromatography–tandem mass spectrometry approach for determining glycosidic linkages. Anal Chem. (2018) 90:13073–80, 10.1021/acs.analchem.8b04124, 30299929.
22. Lee, H, de MeloSilva, VL, Liu, Y, Barile, D. Short communication: Quantification of carbohydrates in whey permeate products using high-performance anion-exchange chromatography with pulsed amperometric detection. J Dairy Sci. (2015) 98:7644–9. 10.3168/jds.2015-9882, 26364096.
23. Zhang, P, Zhang, Y, Xue, X, Wang, C, Wang, Z, Huang, L. Relative quantitation of glycans using stable isotopic labels 1-(d0/d5) phenyl-3-methyl-5-pyrazolone by mass spectrometry. Anal Biochem. (2011) 418:1–9. 10.1016/j.ab.2011.07.006, 21803021.
24. Walker, SH, Budhathoki-Uprety, J, Novak, BM, Muddiman, DC. Stable-isotope labeled hydrophobic hydrazide reagents for the relative quantification of N-linked glycans by electrospray ionization mass spectrometry. Anal Chem. (2011) 83:6738–45. 10.1021/ac201376q, 21774516.
25. Hahne, H, Neubert, P, Kuhn, K, Etienne, C, Bomgarden, R, Rogers, JC,. Carbonyl-reactive tandem mass tags for the proteome-wide quantification of N-linked glycans. Anal Chem. (2012) 84:3716–24. 10.1021/ac300197c, 22455665.
26. Robinson, RC, Poulsen, NA, Barile, D. Multiplexed bovine milk oligosaccharide analysis with aminoxy tandem mass tags. PLoS ONE. (2018) 13:e0196513. 10.1371/journal.pone.0196513, 29698512.
27. Orlando, R. Quantitative analysis of glycoprotein glycans. In: Kohler, JJ, Patrie, SM, editors. Mass Spectrometry of Glycoproteins: Methods and Protocols Methods in Molecular Biology. Totowa, NJ: Humana Press (2013). p. 197–215. 23296532.
28. Dong, X, Huang, Y, Cho, BG, Zhong, J, Gautam, S, Peng, W,. Advances in mass spectrometry-based glycomics. Electrophoresis. (2018) 39:3063–81. 10.1002/elps.201800273, 30199110.
29. Robinson, RC. Novel Analytical Techniques for Characterization of Health-Promoting Bioactive Peptides and Oligosaccharides in Dairy Products. dissertation. University of California, Davis, Davis, CA. (2019).
30. McJarrow, P, van, Amelsfort-Schoonbeek J. Bovine sialyl oligosaccharides: seasonal variations in their concentrations in milk, and a comparison of the colostrums of Jersey and Friesian cows. Int Dairy J. (2004) 14:571–9. 10.1016/j.idairyj.2003.11.006.
31. Nakamura, T, Kawase, H, Kimura, K, Watanabe, Y, Ohtani, M, Arai, I,. Concentrations of sialyloligosaccharides in bovine colostrum and milk during the prepartum and early lactation. J Dairy Sci. (2003) 86:1315–20. 10.3168/jds.S0022-0302(03)73715-1, 12741556.
32. Barile, D, Tao, N, Lebrilla, CB, Coisson, J-D, Arlorio, M, German, JB. Permeate from cheese whey ultrafiltration is a source of milk oligosaccharides. Int Dairy J. (2009) 19:524–30. 10.1016/j.idairyj.2009.03.008, 20161544.
33. Yang, S-T. Chapter 1. Bioprocessing - from biotechnology to biorefinery. In: Yang, S-T, editor. Bioprocessing for Value-Added Products from Renewable Resources: New Technologies and Applications. Amsterdam: Elsevier (2007). p. 17–8.
34. Paterson, AHJ. Lactose and oligosaccharides: Lactose: Production, applications. In: Fuquay, JW, Fox, PF, McSweeny, PLH, editors. Encyclopedia of Dairy Sciences. Boston: Elsevier, (2011). p. 196–201.
35. de Moura Bell, JMLN, Cohen, JL, de Aquino, LFMC, Lee, H, de Melo Silva, VL, Liu, Y,. An integrated bioprocess to recover bovine milk oligosaccharides from colostrum whey permeate. J Food Eng. (2018) 216:27–35. 10.1016/j.jfoodeng.2017.07.022, 29217872.
36. Cohen, JL, Barile, D, Liu, Y, de Moura Bell, JM. Role of pH in the recovery of bovine milk oligosaccharides from colostrum whey permeate by nanofiltration. Int Dairy J. (2017) 66:68–75. 10.1016/j.idairyj.2016.10.016, 28652648.
37. Factory. Available online at: http://www.publicdomainfiles.com/show_file.php?id=13525908011871. Public domain photo (accessed February 7, 2019).
38. Robinson, RC, Poulsen, NA, Colet, E, Duchene, C, Larsen, LB, Barile, D. Profiling of aminoxyTMT-labeled bovine milk oligosaccharides reveals substantial variation in oligosaccharide abundance between dairy cattle breeds. Sci Rep. (2019) 9:5465. 10.1038/s41598-019-41956-x, 30940931.
39. Liu, Z, Wang, T, Pryce, JE, MacLeod, IM, Hayes, BJ, Chamberlain, AJ,. Fine-mapping sequence mutations with a major effect on oligosaccharide content in bovine milk. Sci Rep. (2019) 9:2137. 10.1038/s41598-019-38488-9, 30765736.
40. Kunz, C, Rudloff, S, Baier, W, Klein, N, Strobel, S. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr. (2000) 20:699–722. 10.1146/annurev.nutr.20.1.699, 10940350.
41. Engfer, MB, Stahl, B, Finke, B, Sawatzki, G, Daniel, H. Human milk oligosaccharides are resistant to enzymatic hydrolysis in the upper gastrointestinal tract. Am J Clin Nutr. (2000) 71:1589–96. 10.1093/ajcn/71.6.1589, 10837303.
42. Gnoth, MJ, Kunz, C, Kinne-Saffran, E, Rudloff, S. Human milk oligosaccharides are minimally digested in vitro. J Nutr. (2000) 130:3014–20. 10.1093/jn/130.12.3014, 11110861.
43. Ruhaak, LR, Stroble, C, Underwood, MA, Lebrilla, CB. Detection of milk oligosaccharides in plasma of infants. Anal Bioanal Chem. (2014) 406:5775–84. 10.1007/s00216-014-8025-z, 25059723.
44. Leoz, MLAD, Wu, S, Strum, JS, Niñonuevo, MR, Gaerlan, SC, Mirmiran, M,. A quantitative and comprehensive method to analyze human milk oligosaccharide structures in the urine and feces of infants. Anal Bioanal Chem. (2013) 405:4089–105. 10.1007/s00216-013-6817-1.
45. Underwood, MA, Gaerlan, S, De Leoz, MLA, Dimapasoc, L, Kalanetra, KM, Lemay, DG,. Human milk oligosaccharides in premature infants: absorption, excretion, and influence on the intestinal microbiota. Pediatr Res. (2015) 78:670–7. 10.1038/pr.2015.162, 26322410.
46. Rudloff, S, Pohlentz, G, Diekmann, L, Egge, H, Kunz, C. Urinary excretion of lactose and oligosaccharides in preterm infants fed human milk or infant formula. Acta Paediatr. (1996) 85:598–603. 10.1111/j.1651-2227.1996.tb14095.x.
47. Lin, AE, Autran, CA, Espanola, SD, Bode, L, Nizet, V. Human milk oligosaccharides protect bladder epithelial cells against uropathogenic Escherichia coli invasion and cytotoxicity. J Infect Dis. (2014) 209:389–98. 10.1093/infdis/jit464, 23990566.
48. Jacobi, SK, Yatsunenko, T, Li, D, Dasgupta, S, Robert, KY, Berg, BM,. Dietary isomers of sialyllactose increase ganglioside sialic acid concentrations in the corpus callosum and cerebellum and modulate the colonic microbiota of formula-fed piglets. J Nutr. (2016) 146:200–8. 10.3945/jn.115.220152, 26701794.
49. Wang, B, Yu, B, Karim, M, Hu, H, Sun, Y, McGreevy, P,. Dietary sialic acid supplementation improves learning and memory in piglets. Am J Clin Nutr. (2007) 85:561–9. 10.1093/ajcn/85.2.561, 17284758.
50. Morgan, BLG, Winick, M. Effects of administration of N-acetylneuraminic acid (NANA) on brain NANA content and behavior. J Nutr. (1980) 110:416–24. 10.1093/jn/110.3.416, 7359212.
51. Vázquez, E, Barranco, A, Ramírez, M, Gruart, A, Delgado-García, JM, Martínez-Lara, E,. Effects of a human milk oligosaccharide, 2′-fucosyllactose, on hippocampal long-term potentiation and learning capabilities in rodents. J Nutr Biochem. (2015) 26:455–65. 10.1016/j.jnutbio.2014.11.016, 25662731.
52. Ruiz-Moyano, S, Totten, SM, Garrido, DA, Smilowitz, JT, German, JB, Lebrilla, CB,. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl Environ Microbiol. (2013) 79:6040–9. 10.1128/AEM.01843-13, 23892749.
53. Sela, DA, Chapman, J, Adeuya, A, Kim, JH, Chen, F, Whitehead, TR,. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci USA. (2008) 105:18964–9. 10.1073/pnas.0809584105, 19033196.
54. Hamilton, MK, Ronveaux, CC, Rust, BM, Newman, JW, Hawley, M, Barile, D,. Prebiotic milk oligosaccharides prevent development of obese phenotype, impairment of gut permeability, and microbial dysbiosis in high fat-fed mice. Am J Physiol: Gastrointest Liver Physiol. (2017) 312:G474–87. 10.1152/ajpgi.00427.2016, 28280143.
55. Jena, PK, Sheng, L, Nagar, N, Wu, C, Barile, D, Mills, DA,. Synbiotics Bifidobacterium infantis and milk oligosaccharides are effective in reversing cancer-prone nonalcoholic steatohepatitis using western diet-fed FXR knockout mouse models. J Nutr Biochem. (2018) 57:246–54. 10.1016/j.jnutbio.2018.04.007, 29800811.
56. Scott, KP, Martin, JC, Duncan, SH, Flint, HJ. Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. FEMS Microbiol Ecol. (2014) 87:30–40. 10.1111/1574-6941.12186, 23909466.
57. Topping, DL, Clifton, PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. (2001) 81:1031–64. 10.1152/physrev.2001.81.3.1031, 11427691.
58. Wong, JMW, de Souza, R, Kendall, CWC, Emam, A, Jenkins, DJA. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. (2006) 40:235–43. 10.1097/00004836-200603000-00015, 16633129.
59. Marcobal, A, Barboza, M, Sonnenburg, ED, Pudlo, N, Martens, EC, Desai, P,. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe. (2011) 10:507–14. 10.1016/j.chom.2011.10.007, 22036470.
60. Samuel, BS, Gordon, JI. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci USA. (2006) 103:10011–6. 10.1073/pnas.0602187103, 16782812.
61. Sheng, L, Jena, PK, Hu, Y, Liu, H-X, Nagar, N, Kalanetra, KM,. Hepatic inflammation caused by dysregulated bile acid synthesis is reversible by butyrate supplementation. J Pathol. (2017) 243:431–41. 10.1002/path.4983, 28892150.
62. Charbonneau, MR, O'Donnell, D, Blanton, LV, Totten, SM, Davis, JC, Barratt, MJ,. Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell. (2016) 164:859–71. 10.1016/j.cell.2016.01.024, 26898329.
63. Obesity and overweight Fact Sheet. World Health Organization (2018). Available online at: https://www.who.int/en/news-room/fact-sheets/detail/obesity-and-overweight (accessed January 15, 2019).
64. Hamilton, MK, Boudry, G, Lemay, DG, Raybould, HE. Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent. Am J Physiol: Gastrointest Liver Physiol. (2015) 308:G840–51. 10.1152/ajpgi.00029.2015, 25747351.
65. Cani, PD, Rodrigo, B, Knauf, C, Waget, A, Neyrinck, AM, Delzenne, NM,. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. (2008) 57:1470–81. 10.2337/db07-1403, 18305141.
66. Ridaura, VK, Faith, JJ, Rey, FE, Cheng, J, Duncan, AE, Kau, AL,. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. (2013) 341:1241214. 10.1126/science.1241214, 24009397.
67. Turnbaugh, PJ, Ley, RE, Mahowald, MA, Magrini, V, Mardis, ER, Gordon, JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. (2006) 444:1027–31. 10.1038/nature05414, 17183312.
68. Teixeira, TFS, Collado, MC, Ferreira, CLLF, Bressan, J, Peluzio, M, do, CG. Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr Res. (2012) 32:637–47. 10.1016/j.nutres.2012.07.003, 23084636.
69. Boudry, G, Hamilton, MK, Chichlowski, M, Wickramasinghe, S, Barile, D, Kalanetra, KM,. Bovine milk oligosaccharides decrease gut permeability and improve inflammation and microbial dysbiosis in diet-induced obese mice. J Dairy Sci. (2017) 100:2471–81. 10.3168/jds.2016-11890, 28131576.
70. Cani, PD, Neyrinck, AM, Fava, F, Knauf, C, Burcelin, RG, Tuohy, KM,. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. (2007) 50:2374–83. 10.1007/s00125-007-0791-0, 17823788.
71. Griffiths, EA, Duffy, LC, Schanbacher, FL, Qiao, H, Dryja, D, Leavens, A,. In vivo effects of bifidobacteria and lactoferrin on gut endotoxin concentration and mucosal immunity in Balb/c mice. Dig Dis Sci. (2004) 49:579–89. 10.1023/B:DDAS.0000026302.92898.ae, 15185861.
72. Jena, PK, Sheng, L, Liu, H-X, Kalanetra, KM, Mirsoian, A, Murphy, WJ,. Western diet–induced dysbiosis in farnesoid X receptor knockout mice causes persistent hepatic inflammation after antibiotic treatment. Am J Pathol. (2017) 187:1800–13. 10.1016/j.ajpath.2017.04.019, 28711154.
73. Gerber Good Start Gentle (HMO) Powder Infant Formula. Available online at: https://www.gerber.com/gerber-good-start-gentle-powder-formula (accessed February 5, 2019).
74. Similac Pro-Advance. Available online at: https://similac.com/baby-formula/pro-advance (accessed February 5, 2019).
75. Chen, X. Chapter four - Human milk oligosaccharides (HMOS): Structure, function, and enzyme-catalyzed synthesis. In: Baker, DC, Horton, D, editors. Advances in Carbohydrate Chemistry and Biochemistry. Waltham, MA: Academic Press (2015). p. 113–90.
76. Smilowitz, JT, Lemay, DG, Kalanetra, KM, Chin, EL, Zivkovic, AM, Breck, MA,. Tolerability and safety of the intake of bovine milk oligosaccharides extracted from cheese whey in healthy human adults. J Nutr Sci. (2017) 6:e6. 10.1017/jns.2017.2, 28620481.
77. Elison, E, Vigsnaes, LK, Krogsgaard, LR, Rasmussen, J, Sørensen, N, McConnell, B,. Oral supplementation of healthy adults with 2′-O-fucosyllactose and lacto-N-neotetraose is well tolerated and shifts the intestinal microbiota. Br J Nutr. (2016) 116:1356–68. 10.1017/S0007114516003354, 27719686.