Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-25T16:17:41.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolution of milk oligosaccharides and lactose: a hypothesis

Published online by Cambridge University Press:  26 July 2011

T. Urashima ,
K. Fukuda  and
M. Messer
T. Urashima*
Affiliation:
Department of Animal Hygiene, Graduate School of Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555, Japan
K. Fukuda
Affiliation:
Department of Animal Hygiene, Graduate School of Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555, Japan
M. Messer
Affiliation:
School of Molecular Biosciences, University of Sydney, NSW2006, Australia
*
†E-mail: [email protected]
Get access

Abstract

Mammalian milk or colostrum contains up to 10% of carbohydrate, of which free lactose usually constitutes more than 80%. Lactose is synthesized within lactating mammary glands from uridine diphosphate galactose (UDP-Gal) and glucose by a transgalactosylation catalysed by a complex of β4-galactosyltransferase and α-lactalbumin (α-LA). α-LA is believed to have evolved from C-type lysozyme. Mammalian milk or colostrum usually contains a variety of oligosaccharides in addition to free lactose. Each oligosaccharide has a lactose unit at its reducing end; this unit acts as a precursor that is essential for its biosynthesis. It is generally believed that milk oligosaccharides act as prebiotics and also as receptor analogues that act as anti-infection factors. We propose the following hypothesis. The proto-lacteal secretions of the primitive mammary glands of the common ancestor of mammals contained fat and protein including lysozyme, but no lactose or oligosaccharides because of the absence of α-LA. When α-LA first appeared as a result of its evolution from lysozyme, its content within the lactating mammary glands was low and lactose was therefore synthesized at a slow rate. Because of the presence of glycosyltransferases, almost all of the nascent lactose was utilized for the biosynthesis of oligosaccharides. The predominant saccharides in the proto-lacteal secretions or primitive milk produced by this common ancestor were therefore oligosaccharides rather than free lactose. Subsequent to this initial period, the oligosaccharides began to serve as anti-infection factors. They were then recruited as a significant energy source for the neonate, which was achieved by an increase in the synthesis of α-LA. This produced a concomitant increase in the concentration of lactose in the milk, and lactose therefore became an important energy source for most eutherians, whereas oligosaccharides continued to serve mainly as anti-microbial agents. Lactose, in addition, began to act as an osmoregulatory molecule, controlling the milk volume. Studies on the chemical structures of the milk oligosaccharides of a variety of mammalian species suggest that human milk or colostrum is unique in that oligosaccharides containing lacto-N-biose I (LNB) (Gal(β1 → 3)GlcNAc, type I) predominate over those containing N-acetyllactosamine (Gal(β1 → 4)GlcNAc, type II), whereas in other species only type II oligosaccharides are found or else they predominate over type I oligosaccharides. It can be hypothesized that this feature may have a selective advantage in that it may promote the growth of beneficial colonic bacteria, Bifidobacteria, in the human infant colon.

Keywords

lactosemilk oligosaccharidesα-lactalbuminlysozymelactationprebioticsbifidobacteria
Type
Full Paper
Information
animal , Volume 6 , Issue 3: 61th EAAP Annual Meeting, 2010, Heraklion, Greece: 10th International Workshop on Biology of Lactation in Farm Animals (BOLFA) and Session “Evolution of mammary gland and milk secretion: consequences for lactation in farm animals” , 27 January 2012 , pp. 369 - 374
Copyright
Copyright © The Animal Consortium 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albrecht, S, Schols, HA, van den Heuvel, EGHM, Voragen, AGJ, Gruppen, H 2010. CE-LIF-MSn profiling of oligosaccharides in human milk and feces of breast-fed babies. Electrophoresis 31, 1264–1273.CrossRefGoogle ScholarPubMed
Amano, J, Messer, M, Kobata, A 1985. Structures of the oligosaccharides isolated from milk of the platypus. Glycoconjugate Journal 2, 121–135.CrossRefGoogle Scholar
Asakuma, S, Nakamura, T, Kimura, K, Watanabe, Y, Akahori, M, Ohbaysahi, H, Arai, I, Sanai, I, Urashima, T 2008. Determination of major neutral oligosaccharide content of human colostrum. European Journal of Clinical Nutrition 62, 488–494.CrossRefGoogle Scholar
Blackburn, DG, Hayssen, V, Muphy, CJ 1989. The origin of lactation and the evolution of milk: A review with new hypotheses. Mammal Review 19, 1–26.CrossRefGoogle Scholar
Brand-Miller, JC, McVeagh, P, McNeil, Y, Messer, M 1998. Digestion of human milk oligosaccharides by healthy infants evaluated by the lactulose hydrogen breath test. Journal of Pediatrics 133, 95–98.CrossRefGoogle ScholarPubMed
Cervantes, LE, Newburg, DS, Ruiz-Palacios, GM 1995. α1–2Fucosylated chains (H-2 and Lewis b) are main human receptor analogues for Campylobacter. Pediatric Research 37, 171A (abstract).Google Scholar
Cravioto, A, Fello, A, Villanfan, H, Ruiz, J, del Vedovo, S, Neeser, JR 1991. Inhibition of localized adhesion of enteropathogenic Escherichia coli to HEp-2 cells by immunoglobulin and oligosaccharide fractions of human colostrum and breast milk. Journal of Infectious Diseases 163, 1247–1255.CrossRefGoogle ScholarPubMed
Engfer, MB, Stahl, B, Finke, B, Sawatzki, G, Daniel, H 2000. Human milk oligosaccharides are resistant to enzymatic hydrolysis in the upper gastrointestinal tract. American Journal of Clinical Nutrition 71, 1589–1596.CrossRefGoogle ScholarPubMed
Gopal, PK, Gill, HS 2000. Oligosaccharides and glycoconjugates in bovine milk and colostrum. British Journal of Nutrition 84 (Suppl. 1), S69–S74.CrossRefGoogle ScholarPubMed
Gyorgy, P, Kuhn, R, Rose, CS, Zilliken, F 1954. Bifidus factor I. A variant of Lactobacillus bifidus requiring a special growth factor. Archives of Biochemistry and Biophysics 48, 193–201.CrossRefGoogle Scholar
Hayssen, V, Blackburn, DG 1985. α-Lactalbumin and the origins of lactation. Evolution 39, 1147–1149.Google ScholarPubMed
Kitaoka, M, Tian, J, Nishimoto, M 2005. Novel putative galactose operon involving lacto-N-biose phosphorylase in Bifidobacterium longum. Applied and Environmental Microbiology 71, 3158–3162.CrossRefGoogle ScholarPubMed
Kobata, A 2010. Structures and application of oligosaccharides in human milk. Proceedings of the Japan Academy, Series B 86, 731–747.CrossRefGoogle ScholarPubMed
Martin, MJ, Martin-Sosa, S, Hueso, P 2002. Binding of milk oligosaccharides by several enterotoxigenic Escherichia coli strains isolated from calves. Glycoconjugate Journal 19, 5–11.CrossRefGoogle ScholarPubMed
Messer, M, Kerry, KR 1973. Milk carbohydrates of the echidna and the platypus. Science 180, 201–203.CrossRefGoogle ScholarPubMed
Messer, M, Trifonoff, E, Stern, W, Collins, JG, Bradbury, JH 1980. Structure of a marsupial-milk trisaccharide. Carbohydrate Research 83, 327–334.CrossRefGoogle Scholar
Messer, M, Trifonoff, E, Collins, JG, Bradbury, JH 1982. Structure of a branched tetrasaccharide from marsupial milk. Carbohydrate Research 102, 316–320.CrossRefGoogle ScholarPubMed
Messer, M, Crisp, EA, Czolij, R 1989. Lactose digestion in suckling macropodids. In Kangaroos, Wallabies and Rat Kangaroos (ed. G Grigg, P Jarman and I Hume ) pp. 217–221, Surry Beatty & Sons Pty Ltd. NSW, Australia.Google Scholar
Messer, M, Griffiths, M, Rismiller, P, Shaw, DC 1997. Lactose synthesis in a monotreme, the echidna (Tachyglossus aculeatus): isolation and amino acid sequence of echidna α-lactalbumin. Comparative Biochemistry and Physiology 118B, 403–410.CrossRefGoogle Scholar
Messer, M, Urashima, T 2002. Evolution of milk oligosaccharides and lactose. Trends in Glycoscience and Glycotechnology 14, 153–176.CrossRefGoogle Scholar
Newburg, DS, Pickering, LK, McCluer, RM, Cleary, TG 1990. Fucosylated oligosaccharides of human milk protect suckling mice from heat-stable enterotoxin of Escherichia coli. Journal of Infectious Diseases 162, 1075–1080.CrossRefGoogle ScholarPubMed
Ninonuevo, MR, Park, Y, Yin, H, Zhang, J, Ward, RE, Clowers, BH, German, JB, Freeman, SL, Killeen, K, Grimm, R, Lebrilla, CB 2006. A strategy for annotating the human milk glycome. Journal of Agriculture and Food Chemistry 54, 7471–7480.CrossRefGoogle ScholarPubMed
Sela, DA, Chapman, J, Adeuya, A, Kim, JH, Chen, F, Whitehead, TR, Lapidus, A, Rokhsar, DS, Lebrilla, CB, German, JB, Price, NP, Richardson, PM, Mills, DA 2008. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proceedings of the National Academy of Sciences of the United States of America 105, 18964–18969.CrossRefGoogle ScholarPubMed
Shaw, DC, Messer, M, Scrivener, AM, Nicholas, KR, Griffiths, M 1993. Isolation, partial characterization, and amino acid sequence of α-lactalbumin from platypus (Ornithorhynchus anatinus) milk. Biochimica et Biophysica Acta 1161, 177–186.CrossRefGoogle ScholarPubMed
Stewart, IM, Messer, M, Walcott, PJ, Gadiel, PA, Griffiths, M 1983. Intestinal glycosidase activities in one adult and two suckling echidnas: absence of a neutral lactase (β-D-galactosidase). Australian Journal of Biological Sciences 36, 139–146.CrossRefGoogle ScholarPubMed
Urashima, T, Saito, T, Nakamura, T, Messer, M 2001. Oligosaccharides of milk and colostrum in non-human mammals. Glycoconjugate Journal 18, 357–371.CrossRefGoogle ScholarPubMed
Urashima, T, Asakuma, S, Messer, M 2007. Milk oligosaccharides. In Comprehensive glycoscience (ed. JP Kamerling, GJ Boons, YC Lee, A Suzuki, N Taniguchi and AGJ Voragen), vol. 4, pp. 695–724. Elsevier, Amsterdam, Netherlands.CrossRefGoogle Scholar
Urashima, T, Odaka, G, Asakuma, S, Uemura, Y, Goto, K, Senda, A, Saito, T, Fukuda, K, Messer, M, Oftedal, OT 2009. Chemical characterization of oligosaccharides in chimpanzee, bonobo, gorilla, orangutan, and siamang milk or colostrum. Glycobiology 19, 499–508.CrossRefGoogle ScholarPubMed
Urashima, T, Kitaoka, M, Terabayashi, T, Fukuda, K, Ohnishi, M, Kobata, K 2011. Milk oligosaccharides. In Oligosaccharides: sources, properties and applications (ed. NG Gordon), pp. 1–58, Nova Science Publishers, New York, USA.Google Scholar
Vorbach, C, Capecci, MR, Penninger, JM 2006. Evolution of the mammary gland from the innate immune system? Bioassays 28, 606–616.CrossRefGoogle ScholarPubMed
Wada, J, Ando, T, Kiyohara, M, Ashida, H, Kitaoka, M, Yamagichi, M, Kumagai, H, Katayama, T, Yamamoto, K 2008. Lacto-N-biosidase from Bifidobacterium bifidum, a critical enzyme for the degradation of human milk oligosaccharides with a type-I structure. Applied and Environmental Microbiology 74, 3996–4004.CrossRefGoogle Scholar
Walcott, PJ, Messer, M 1980. Intestinal lactase (β-galactosidase) and other glycosidase activities in suckling and adult tammar wallabies (Macropus engenii). Australian Journal of Biological Science 32, 521–530.CrossRefGoogle Scholar