Skip to main content
SpringerLink
Log in

Characterization of two novel sialyl N-acetyllactosaminyl nucleotides separated from ovine colostrum

  • Original Article
  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

The milk/colostrum of some mammalian species is known to contain sugar nucleotides including uridine diphosphate (UDP) oligosaccharides in addition to lactose and milk oligosaccharides, but the detailed structures of these UDP oligosaccharides have not so far been clarified. In this study we isolated two UDP-sialyl N-acetyllactosamines from ovine colostrum and characterized them using 1H-NMR and MALDI-TOFMS spectroscopies. Their structures were found to be Neu5Gc(α2–3)Gal(β1–4)GlcNAcα1-UDP and Neu5Gc(α2–6)Gal(β1–4)GlcNAcα1-UDP.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Jenness R.E., Regehr E.A., Sloan R.E.: Comparative studies of milks. II. Dialyzable carbohydrates. Comp. Biochem. Physiol. 13, 339–352 (1964)

    Article  CAS  PubMed  Google Scholar 

  2. Ursshima T., Asakuma S., Messer M.: Milk oligosaccharides. In: Kamehring J.P.Y. (ed.) Comprehensive glycoscience, pp. 695–724. Elsevier, Amsterdam (2007)

    Chapter  Google Scholar 

  3. Urashima T., Saito T., Nakamura T., Messer M.: Oligosaccharides of milk and colostrum in non-human mammsla. Glycoconj. J. 18, 357–371 (2001)

    Article  CAS  PubMed  Google Scholar 

  4. Urashima T., Messer M., Oftedal O.T.: Comparative biochemistry and evolution of milk oligosaccharides of monotremes, marsupials and eutherians. In: Pontaritti P. (ed.) Evolutionary biology, genome evolution, speciation, coevolution and origin of life, pp. 3–33. Springer, Switzerland (2014)

  5. Engfer M.B., 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. 71, 1589–1596 (2000)

    CAS  PubMed  Google Scholar 

  6. Urashima T., Kitaoka M., Asakuma S., Messer M.: Milk oligosaccharides. In: McSweeney P.H.L., Fox P.P. (eds.) Advanced dairy chemistry, vol. 3, 3rd edn, pp. 295–349. Springer Science + Business Media, New York (2009)

    Chapter  Google Scholar 

  7. Urashima T., Asakuma S., Kitaoka M., Messer M.: Indigenous oligosaccharides in milk. In: Fuquay Q.W., Fox P.P., McSweeney P.H.L. (eds.) Encyclopedia of dairy science, vol. 3, 2nd edn, pp. 241–273. Academic Press, New York (2011)

    Chapter  Google Scholar 

  8. Urashima T., Kitaoka M., Terabayashi T., Fukuda K., Onnishi M., Kobata A.: Milk oligosaccharides. In: Grodon N.S. (ed.) Oligosaccharides: sources, properties and applications, pp. 1–58. Nova Science, New York (2011)

    Google Scholar 

  9. Bubb W.A., Ursshima T., Kohso K., Nakamura T., Arai I., Saito T.: Occurrence of an unusual lactose sulfate in dog milk. Carbohydr. Res. 318, 123–128 (1999)

    Article  CAS  PubMed  Google Scholar 

  10. Sturman J.A., Lin Y.Y., Higuchi T., Fellmen J.H.: N-Acetylneuramin lactose sulfate: a newly identified nutrient in milk. Pediatr. Res. 19, 216–219 (1985)

    Article  CAS  PubMed  Google Scholar 

  11. Urashima T., Nakamura T., Nakagawa D., Noda M., Arai I., Saito T., Lydersen C., Kovacs K.M.: Characterization of oligosaccharides in milk of bearded seal (Erignathus barbatus). Comp. Biochem. Physiol. B138, 1–18 (2004)

    Article  Google Scholar 

  12. Kinoshita M., Ohta H., Higaki K., Kojima Y., Urashima T., Nakajima K., Suzuki M., Kovacs K.M., Lydersen C., Hayakawa T., Kakehi K.: Structural characterization of multi-branched oligosaccharides from seal milk by combination of off-line HPLC-MALDI-TOF MS and sequential exoglycosidase digestion. Anal. Biochem. 388, 242–253 (2009)

    Article  CAS  PubMed  Google Scholar 

  13. Goto K., Fukuda K., Senda A., Saito T., Kimura K., Glander K.F., Hinde K., Dittus W., Milligan L.A., Power M.L., Oftedal O.T., Urashima T.: Chemical characterization of oligosaccharides in the milk of six species of new and old world monkeys. Glycoconj. J. 27, 703–715 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Taufik E., Fukuda K., Senda A., Saito T., Williams C., Tilden C., Eisert R., Oftedal O.T., Urashima T.: Structural characterization of neutral and acidic oligosaccharides in milks of strepsirrhine primates: greater galago, aye-aye. Coquerel’s sifaka and mongoose lemur. Glyconj. J. 29, 119–134 (2012)

  15. Guerrardel Y., Morelle W., Plancke Y., Lemoine J., Strecker J.: Structural analysis of three sulfated oligosaccharides isolated from human milk. Carbohydr. Res. 320, 230–238 (1999)

    Article  Google Scholar 

  16. Anraku T., Fukuda K., Saito T., Messer M., Urashima T.: Chemical characterization of acidic oligosaccharides in milk of the red kangaroo (Macropus rufus). Glyconj. J. 29, 147–156 (2012)

    Article  CAS  Google Scholar 

  17. Urashima T., Fujita S., Fukuda K., Nakamura T., Saito T., Cowan P., Messer M.: Chemical characterization of milk oligosaccharides of the common brushtail possum (Trichosurus vulpecula). Glycoconj. J. 31, 387–399 (2014)

    Article  CAS  PubMed  Google Scholar 

  18. Hirayama K., Taufik E., Kikuchi M., Nakamura T., Fukuda K., Saito T., Newgrain K., Green B., Messer M., Urashima T.: Chemical characterization of milk oligosaccharides of the common wombat (Vombatus ursinus). Anim. Sci. J (2016). doi:10.1111/asj.12566

  19. Urashima T., Sun Y., Fukuda K., Hirayama K., Taufik E., Nakamura T., Saito T., Merchant J., Green B., Messer M.: Chemical characterization of milk oligosaccharides of the eastern quoll (Dasyurus viverrinus). Glcyconj. J. 32, 361–370 (2015)

    Article  CAS  Google Scholar 

  20. Nakamura T., Amikawa S., Harada T., Saito T., Arai I., Urashima T.: Occurrence of an unusual phosphorylated N-acetyllactosamine in horse colostrum. Biochim. Biophys. Acta. 1425, 13–18 (2001)

    Article  Google Scholar 

  21. Parkkinen J., Finne J.: Isolation of sialyl oligosaccharides and sialyl oligosaccharide phosphates from bovine colostrum and human urine. Methods Enzymol. 138, 289–300 (1987)

    Article  CAS  PubMed  Google Scholar 

  22. Albrecht S., Lane J.A., Marino K., Al Busadah K.A., Carrington S.D., Hickey R.M., Rudd P.M.: A comparative study of free oligosaccharides in the milk of domestic animals. Br. J. Nutr. 111, 1313–1328 (2014)

    Article  CAS  PubMed  Google Scholar 

  23. Kobata A.: The acid soluble nucleotides of milk. II. Isolation and identification of two novel uridine nucleotides of oligosaccharide conjugates from human milk and colostrum. J. Biochem. Tokyo. 53, 167–175 (1963)

    CAS  Google Scholar 

  24. Kobata A.: The acid soluble nucleotides of milk. IV. The chemical structure of UDP-X3. J. Biochem. Tokyo. 59, 63–66 (1966)

    CAS  PubMed  Google Scholar 

  25. Jourdian G.W., Shimizu F., Roseman S.: Isolation of nucleotide – oligosaccharides containing sialic acid. Fed. Proc. 20, 161 (1961)

    Google Scholar 

  26. Kobata A., Suzuki Z.: The acid – soluble nucleotides of milk. III. Occurrence of UDP-N-acetyllactosamine and UDP-D-xylose in pig’s milk and colostrum. Biochim. Biophys. Ata. 107, 405–413 (1965)

    CAS  Google Scholar 

  27. Taufik E., Ganzorig K., Nanslmaa M., Fukuda R., Fukuda K., Saito T., Urashima T.: Chemical characterization of saccharides in the milk of a reindeer (Rangufer tarandus tarandus). Int. Dairy J. 34, 104–108 (2014)

    Article  CAS  Google Scholar 

  28. Urashima T., Saito T., Nishimura J., Ariga H.: New galactosyllactose containing α-glycosidic linkage isolated from ovine (Booroola dorset) colostrum. Biochim. Biophys. Acta. 992, 375–378 (1989)

    Article  CAS  PubMed  Google Scholar 

  29. Nakamura T., Urashima T., Nakagawa M., Saito T.: Sialyllactose occurs as free lactones in ovine colostrum. Biochim. Biophy. Acta. 1381, 286–292 (1998)

    Article  CAS  Google Scholar 

  30. Dubois M., Gills K.A., Hamilton J.K., Roberts P.A., Smith F.: Colorimetric method for determinetion of sugars and related substances. Anal. Chem. 28, 350–356 (1956)

    Article  CAS  Google Scholar 

  31. Jourdian G.W., Dean L., Roseman S.: The sialic acid XI. A periodate – resorcinol method for the quantitative estimation of free sialic acids and their glycosides. J. Biol. Chem. 256, 430–435 (1971)

    Google Scholar 

  32. Zervosen A., Nieder V., Gallego R.G., Kamerling J.P., Vliegenthart J.F.G., Elling L.: Synthesis of nucleotide – activated oligosaccharides by β-galactosidase from Bacillus circulans. Biol. Chem. 382, 299–311 (2001)

    Article  CAS  PubMed  Google Scholar 

  33. Garrido D., Barile D., Mills D.A.: A molecular basis for Bifidobacterial enrichment in the infant gastrointestinal tract. Adv. Nutr. 3, 415S–421S (2012)

  34. Lane J.A., Marino K., Naughton J., Kavanaugh D., Clyne M., Carrington S.D., Hickey R.M.: Anti-infective bovine colostrum oligosaccharides: Campylobacter jejuni as a case study. Int. J. Food Microbiol. 157, 182–188 (2012)

    Article  CAS  PubMed  Google Scholar 

  35. Hester S.N., Chen X., Li M., Monaco M.H., Comstock S.S., Kuhlenschmidt T.B., Kuhlenschmidt M.S., Donovan S.M.: Human milk oligosaccharides inhibit rotavirus infectivity in vitro and in acutely infected piglets. Br. J. Nutr. 110, 1233–1242 (2013)

    Article  CAS  PubMed  Google Scholar 

  36. Holscher H.D., Davis S.R., Tappenden K.A.: Human milk oligosaccharides influence maturation of human intestinal Caco-2 Bbe and HT-29 cell lines. J. Nutr. 144, 586–591 (2014)

    Article  CAS  PubMed  Google Scholar 

  37. Lane J.A., O’Callaghan J., Carrington S.T., Hickey R.M.: Transcriptional response of HT-29 intestinal epitherial cells to human and bovine milk oligosaccharides. Br. J. Nutr. 110, 2127–2137 (2013)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

This study was partially supported by financial aid from the Yotsuba Milk Products Company.

Author information

Authors and Affiliations

  1. Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture & Veterinary Medicine, Obihiro, Hokkaido, 080-8555, Japan

    Masashi Sasaki, Kentaro Hirayama, Kenji Fukuda & Tadasu Urashima

  2. Department of Food Science, Obihiro University of Agriculture & Veterinary Medicine, Obihiro, Hokkaido, 080-8555, Japan

    Tadashi Nakamura

  3. Graduate School of Agriculture, Tohoku University, Sendai, Miyagi, 981-8555, Japan

    Tadao Saito

  4. Intensive Grazing Research Team, National Agricultural Research Center for Hokkaido Region, Sapporo, Hokkaido, 062-8555, Japan

    Sadaki Asakuma

Authors
  1. Masashi Sasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tadashi Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kentaro Hirayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kenji Fukuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tadao Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tadasu Urashima
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sadaki Asakuma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tadasu Urashima.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sasaki, M., Nakamura, T., Hirayama, K. et al. Characterization of two novel sialyl N-acetyllactosaminyl nucleotides separated from ovine colostrum. Glycoconj J 33, 789–796 (2016). https://doi.org/10.1007/s10719-016-9672-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-016-9672-4

Keywords

Search

Navigation