Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-25T01:35:25.537Z Has data issue: false hasContentIssue false
  • English
  • Français

Lactose-derived oligosaccharides in the milk of elephants: comparison with human milk

Published online by Cambridge University Press:  19 January 2010

Clemens Kunz ,
Silvia Rudloff ,
Wolfgang Schad  and
Daniel Braun
Clemens Kunz*
Affiliation:
Research Institute of Child Nutrition, Heinstück 11, 44225 Dortmund, Germany
Silvia Rudloff
Affiliation:
Research Institute of Child Nutrition, Heinstück 11, 44225 Dortmund, Germany
Wolfgang Schad
Affiliation:
Institute for Evolutionary Biology and Morphology, University of Witten/Herdecke, Stockumer Str. 10, 58448 Witten, Germany
Daniel Braun
Affiliation:
Institute for Evolutionary Biology and Morphology, University of Witten/Herdecke, Stockumer Str. 10, 58448 Witten, Germany
*
* Dr Clemens Kunz, fax +49 99 39 049, email [email protected]
Rights & Permissions [Opens in a new window]

Extract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Human milk is commonly considered to be unique when compared with the milk of other species with regard to its high content of complex fucosylated and sialylated lactose-derived oligosaccharides. We describe the application of high-pH anion-exchange chromatography with pulsed amperometric detection and TLC to characterize and quantitate neutral and sialylated lactose-derived oligosaccharides in milk from three Asian elephants and human milk. The lactose contents of elephant and human milks were 25–30 g/l and about 66 g/l respectively, whereas total oligosaccharide concentration was about three times higher in elephant milk and comprised up to 40% (10% in human milk) of the carbohydrate content. The ratio neutral: acidic components was different in the milk of the two species; in elephant milk, the N-acetylneuraminic acid-containing oligosaccharides made up almost half of the total amount v. 30% in human milk. Most oligosaccharides in elephant milk were more fucosylated and/or sialylated compared with human milk components. By mild acid hydrolysis, fucose and N-acetylneuraminic acid were cleaved off from complex components, and this resulted in increased amounts of fucose, galactose, N-acetylneuraminic acid, lactose and lacto-N-neo-tetraose. Unique to elephant milk are the high levels of 3′-galactosyllactose (up to 4 g/l) and lacto-N-neo-tetraose which are present in human milk only in trace amounts. Elephant and human milks have high levels and unique patterns of oligosaccharides which may reflect the relative importance of these components in neonatal host defence, in endothelial leucocyte interactions or in brain development.

Type
Research Article
Information
British Journal of Nutrition , Volume 82 , Issue 5 , November 1999 , pp. 391 - 399
Copyright
Copyright © The Nutrition Society 1999

References

Bergman, HC & Housley, C (1968) Chemical analysis of American opossum (Didelphis virginiana) milk. Comparative Biochemistry and Physiology 25, 213–218.CrossRefGoogle Scholar
Braun, D (1997) Die Milchkompositionen der Saugetiere im Vergleich und die Milch des Menschen (Comparison of the milk composition of mammals and the milk of humans). PhD Thesis, University of Witten, Germany.Google Scholar
Carlini, AR, Marquez, MEI, Soave, G, Vergani, DF & Ronayne de Ferrer, PA (1994) Southern elephant seal, Mirounga leonina: composition of milk during lactation. Polar Biology 14, 37–42.CrossRefGoogle Scholar
Carlson, SE (1985) N-acetylneuraminic acid concentrations in human milk oligosaccharides and glycoproteins during lactation. American Journal of Clinical Nutrition 41, 720–726.CrossRefGoogle ScholarPubMed
Carlson, SE & House, SG (1986) Oral and intraperitoneal administration of N-acetylneuraminic acid: effect on rat cerebral and cerebrellar N-acetylneuraminic acid. Journal of Nutrition 116, 881–886.CrossRefGoogle Scholar
Dische, Z (1962) General color reactions. In Methods in Carbohydrate Chemistry, vol. 1, pp. 488–494 [Whistler, RL and Wolfrom, ML, editors]. New York, NY: Academic Press.Google Scholar
Egge, H (1993) The diversity of oligosaccharides in human milk. In New Perspectives in Infant Nutrition, pp. 12–26 [Renner, B and Sawatzki, G, editors]. Stuttgart: Thieme Verlag.Google Scholar
Egge, H, Dell, A & von Nicolai, H (1983) Fucose containing oligosaccharides from human milk. I. Separation and identification of new constituents. Archives of Biochemistry and Biophysics 224, 235–253.CrossRefGoogle ScholarPubMed
Gibson, JB, Berry, GT, Palmieri, MJ, Reynolds, RA, Mazur, AT & Segal, S (1996) Sugar nucleotide concentrations in red blood cells of patients on protein- and lactose-limited diets: effects of galactose supplementation. American Journal of Clinical Nutrition 63, 704–708.CrossRefGoogle ScholarPubMed
Gross, R & Bolliger, A (1958) The occurrence of carbohydrates other than lactose in milk of a marsupial, Trichosurus vulpecula. Australian Journal of Sciences 20, 184–185.Google Scholar
Hardy, MR & Townsend, RR (1988) Monosaccharide analysis of glycoconjugates by anion exchange chromatography with pulsed amperometric detection. Analytical Biochemistry 170, 54–62.CrossRefGoogle ScholarPubMed
Jenness, R, Erickson, AW & Craighead, JJ (1972) Some comparative aspects of milk from four species of bears. Journal of Mammalogy 53, 34–47.CrossRefGoogle ScholarPubMed
Kobata, A (1977) Milk glycoproteins and oligosaccharides. In The Glycoconjugates, vol. 1, pp. 423–440 [Horowitz, MI and Pigman, W, editors]. New York, NY: Academic Press.CrossRefGoogle Scholar
Kunz, C (1999) Microbial receptor analogs in human milk: structural and functional aspects. In Probiotics, Other Nutritional Factors, and Intestinal Microflora, Nestle Nutrition Workshop Series, vol. 42, pp. 157–174 [Hanson, LA and Yolken, RH, editors]. Philadelphia, PA: Lippincott-Raven Publishers.Google Scholar
Kunz, C, Obermeier, S, Rudloff, S, Hartmann, R, Pohlentz, G, Brosicke, H & Lentze, MJ (1999) Stable isotope investigations of the biosynthesis of lactose and oligosaccharides in lactating women. FASEB Journal 13, A 254.Google Scholar
Kunz, C & Rudloff, S (1993) Biological functions of oligosaccharides in human milk. Acta Paediatrica 82, 903–912.CrossRefGoogle ScholarPubMed
Kunz, C, Rudloff, S, Hintelmann, A, Pohlentz, G & Egge, H (1996 a) High-pH anion exchange chromatography with pulsed amperometric detection and molar response factors of human milk oligosaccharides. Journal of Chromatography B 685, 211–221.CrossRefGoogle ScholarPubMed
Kunz, C, Rudloff, S, Pohlentz, G & Egge, H (1996 b) Oligosaccharides in milk of different species including man, rhesus monkey, cow and pig. FASEB Journal 10, A748.Google Scholar
Kunz, C, Rudloff, S, Pohlentz, G, Lönnerdal, B & Egge, H (1993) Sialylated and fucosylated oligosaccharides in rhesus monkey milk. FASEB Journal 7, A 823.Google Scholar
McCullagh, KG, Lincoln, HG & Southgate, DA (1969) Fatty acid corn-position of milk fat of the Asian elephant. Nature 222, 493–494.CrossRefGoogle Scholar
Messer, M & Green, B (1979) Milk carbohydrates of marsupials. I. Quantitative and qualitative changes in milk carbohydrates during lactation in the tammar wallaby (Macropus eugenii). Australian Journal of Biological Sciences 32, 519–531.CrossRefGoogle ScholarPubMed
Messer, M & Kerry, KR (1973) Milk carbohydrates of the echidna and platypus. Science 180, 201–203CrossRefGoogle ScholarPubMed
Messer, M & Mossop, GS (1977) Milk carbohydrates of marsupials. 1. Partial separation and characterization of neutral milk oligosaccharides of the Eastern grey kangaroo. Australian Journal of Biological Sciences 30, 379–388.CrossRefGoogle Scholar
Messer, M & Nicholas, KR (1991) Biosynthesis of marsupial milk oligosaccharides: characterization and developmental changes of two galactosyltransferases in lactating mammary glands of the tammar wallaby, Macropus eugenii. Biochimica et Biophx-sicaActa 1077, 79–85.CrossRefGoogle ScholarPubMed
Messer, M, Trifonoff, E, Stern, W, Grant Collins, J & Howard Bradbury, J (1980) Structure of a marsupial milk trisaccharide. Carbohydrate Research 83, 327–334.CrossRefGoogle ScholarPubMed
Montreuil, J (1993) The saga of human milk gynolactose. In New Perspectives in Infant Nutrition, pp. 3–11 [Renner, B and Sawatzki, G, editors]. Stuttgart: Thieme Verlag.Google Scholar
Montreuil, J & Mullet, S (1960) Etude des variations des constituents glucidiques du lait de femme au cours de la lactation (Study of the variation in sugars of human milk during lactation). Bulletin de la Societe Chimique et Biologique 42, 365–377.Google Scholar
Obermeier, S.Rudloff, S.Brösicke, H, Hartmann, R & Kunz, C (1999) Analysis of 13C-enriched milk, urine and breath of a lactating woman after an oral [l-13C]galactose or [1-13C]glucose bolus. FASEB Journal 13, A254.Google Scholar
Oftedal, OT & Iverson, SI (1995) Comparative analysis of non-human milks. A. Phylogenetic variation in the gross composition of milks. In Handbook of Milk Composition, pp. 749–789 [Jensen, RG, editor]. San Diego, CA: Academic Press.CrossRefGoogle Scholar
Petry, K, Greinix, HT, Nudelman, E, Eisen, H, Hakomori, S-I, Levy, HL & Reichardt, JKV (1991) Characterization of a novel biochemical abnormality in galactosemia: deficiency of glycolipids containing galactose or N-acetylgalactosamine and accumulation of precursors in brain lymphocytes. Biochemical Medicine and Metabolic Biology 46, 93–104.CrossRefGoogle ScholarPubMed
Rudloff, S, Braun, D, Schad, W & Kunz, C (1998) Oligosaccharides in milk - a relationship to brain development? FASEB Journal 12, A235.Google Scholar
Rudloff, S, Pohlentz, G, Diekmann, L, Egge, H & Kunz, C (1996) Urinary excretion of lactose and oligosaccharides in preterm infants fed human milk or infant formula. Acta Paediatrica 85, 598–603.CrossRefGoogle ScholarPubMed
Sadhu, DP (1948) Correlation between the lactose content of milk and the cerebroside and choline content of brain. Journal of Dairy Science 31, 347–351.CrossRefGoogle Scholar
Springer, TA (1990) Adhesion receptors of the immune system. Nature 346, 425–434.CrossRefGoogle ScholarPubMed
Stahl, B, Thurl, S, Zeng, J, Karas, M, Hillenkamp, F, Steup, M & Sawatzki, G (1994) Oligosaccharides from human milk as revealed by matrix-assisted laser desorption/ionization mass spectrometry. Analytical Biochemistry 223, 218–226.CrossRefGoogle ScholarPubMed
Svennerholm, L (1957) Quantitative estimation of sialic acids. II. A colorimetric resorcin hydrochloric acid method. Biochimica et Biophysica Acta 24, 604–611.CrossRefGoogle Scholar
Urashima, T, Kusaka, Y, Nakamura, T, Saito, T, Maeda, N & Messer, M (1997) Chemical characterization of milk oligosaccharides of the brown bear, Ursus arctos yesoensis. Biochimica et Biophysica Acta 1334, 247–255.CrossRefGoogle ScholarPubMed
Urashima, T, Saito, T, Nishimura, J & Ariga, H (1989) New galactosyllacotse containing alpha-glycosidic linkage isolated from ovine (Booroola dorset) colostrum. Biochimica et Biophysica Acta 992, 375–378.CrossRefGoogle ScholarPubMed
Urashima, T, Saito, T, Ohmisya, K & Shimazaki, K (1991) Structural determination of three neutral oligosaccharides in bovine (Holstein-Friesian) colostrum, including the novel trisaccharide GaINAcα;l-3Galβ1–4Glc. Biochimica et Biophysica Acta 1073, 225–229.CrossRefGoogle Scholar
Urashima, T, Saito, T, Tsuji, Y, Taneda, Y, Takasawa, T & Messer, M (1994) Chemical characterization of sialyl oligosaccharides isolated from tammar wallaby (Macropus eugenii) milk. Biochimica et Biophysica Acta 1200, 64–72.CrossRefGoogle ScholarPubMed
Witt, W, von Nicolai, H & Zilliken, F (1979) Uptake and distribution of orally applied N-acetyl-(14C)-neuraminyllactose and N-acetyl-(14C)-neuraminic acid in the organs of newborn rats. Nutrition and Metabolism 23, 51–61.CrossRefGoogle Scholar
Zopf, D & Roth, S (1996) Oligosaccharide anti-infective agents. Lancet 347, 1017–1021.CrossRefGoogle ScholarPubMed