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Glycoconjugate Journal

, Volume 35, Issue 3, pp 275–286 | Cite as

Chemical structures of oligosaccharides in milk of the raccoon (Procyon lotor)

  • Tadasu Urashima
  • Emi Yamaguchi
  • Takeharu Ohshima
  • Kenji Fukuda
  • Tadao Saito
Original Article
  • 137 Downloads

Abstract

In this study on milk saccharides of the raccoon (Procyonidae: Carnivora), free lactose was found to be a minor constituent among a variety of neutral and acidic oligosaccharides, which predominated over lactose. The milk oligosaccharides were isolated from the carbohydrate fractions of each of four samples of raccoon milk and their chemical structures determined by 1H-NMR and MALDI-TOF mass spectroscopies. The structures of the four neutral milk oligosaccharides were Fuc(α1–2)Gal(β1–4)Glc (2′-fucosyllactose), Fuc(α1–2)Gal(β1–4)GlcNAc(β1–3)Gal(β1–4)Glc (lacto-N-fucopentaose IV), Fuc(α1–2)Gal(β1–4)GlcNAc(β1–3)Gal(β1–4)GlcNAc(β1–3)Gal(β1–4)Glc (fucosyl para lacto-N-neohexaose) and Fuc(α1–2)Gal(β1–4)GlcNAc(β1–3)[Fuc(α1–2)Gal(β1–4)GlcNAc(β1–6)]Gal(β1–4)Glc (difucosyl lacto-N-neohexaose). No type I oligosaccharides, which contain Gal(β1–3)GlcNAc units, were detected, but type 2 saccharides, which contain Gal(β1–4)GlcNAc units were present. The monosaccharide compositions of two of the acidic oligosaccharides were [Neu5Ac]1[Hex]6[HexNAc]4[deoxy Hex]2, while those of another two were [Neu5Ac]1[Hex]8[HexNAc]6[deoxy Hex]3. These acidic oligosaccharides contained α(2–3) or α(2–6) linked Neu5Ac, non reducing α(1–2) linked Fuc, poly N-acetyllactosamine (Gal(β1–4)GlcNAc) and reducing lactose.

Keywords

Raccoon milk oligosaccharides Milk oligosaccharides Raccoon milk Procyon lotor Carnivora 

Notes

Acknowledgements

This work was supported by a Grant-in-Aid for Scientific Research (C), grant No. 16 K08003, from the Japan Society for the Promotion of Science, Sports and Culture (Japan), and a grant from Yotsuba Milk Products Co (Japan).

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Jenness, R.E., Regehr, E.A., Sloan, R.E.: Comparative studies of milks. II. Dialyzable carbohydrates. Comp. Biochem. Physiol. 13, 339–352 (1964)CrossRefPubMedGoogle Scholar
  2. 2.
    Urashima, T., Saito, T., Nakamura, T., Messer, M.: Oligosaccharides of milk and colostrum in non-human mammals. Glycoconj. J. 18, 357–371 (2001)CrossRefPubMedGoogle Scholar
  3. 3.
    Urashima, T., Messer, M., Oftedal, O.T.: Oligosaccharides in the milk of other mammals. In: McGuire, M., McGuire, M., Bode, L. (eds.) Prebiotics and probiotics in human milk, pp. 45–139. Academic Press, Amsterdam (2016)Google Scholar
  4. 4.
    Messer, M., Urashima, T.: Evolution of milk oligosaccharides and lactose. Trends Glycosci. Glycotechnol. 14, 153–176 (2002)CrossRefGoogle Scholar
  5. 5.
    Urashima, T., Fukuda, K., Kitaoka, M., Ohnishi, M., Terabayashi, T., Kobata, A.: Milk oligosaccharides. In: Gordon, N.S. (ed.) Oligosaccharides, Properties and Applications, pp. 1–58. Nova Science, New York (2011)Google Scholar
  6. 6.
    Urashima, T., Fukuda, K., Messer, M.: Evolution of milk oligosaccharides and lactose: a hypothesis. Animal. 6, 369–374 (2012)CrossRefPubMedGoogle Scholar
  7. 7.
    Urashima, T., Messer, M., Oftedal, O.T.: Comparative biochemistry and evolution of milk oligosaccharides of monotremes, marsupials, and eutherians. In: Pontarotti, P. (ed.) Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life, pp. 3–33. Springer, Swizerland (2014)Google Scholar
  8. 8.
    Urashima, T., Messer, M.: Evolution of milk oligosaccharides and their function in monotremes and marsupials. In: Pontarotti, P. (ed.) Evolutionary Biology: Self/Nonself Evolution, Species and Complex Traits Evolution, Methods and Concepts, pp. 237–256. Springer, Swizerland (2017)Google Scholar
  9. 9.
    Urashima, T., Kusaka, Y., Nakamura, T., Saito, T., Maeda, N., Messer, M.: Chemical characterization of milk oligosaccharides of the brown bear, Ursus arctos yesoensis. Biochim. Biophys. Acta. 1334, 247–255 (1997)CrossRefPubMedGoogle Scholar
  10. 10.
    Urashima, T., Sumiyoshi, W., Nakamura, T., Arai, I., Saito, T., Komatsu, T., Tsubota, T.: Chemical characterization of milk oligosaccharides of the Japanese black bear, Ursus thibetanus japonicus. Biochim. Biophys. Acta. 1472, 290–306 (1999)CrossRefPubMedGoogle Scholar
  11. 11.
    Urashima, T., Yamashita, T., Nakamura, T., Arai, I., Saito, T., Derocher, A.E., Wiig, O.: Chemical characterization of milk oligosaccharides of the polar bear, Ursus maritimus. Biochim. Biophys. Acta. 1475, 395–408 (2000)CrossRefPubMedGoogle Scholar
  12. 12.
    Urashima, T., Nagata, H., Nakamura, T., Arai, I., Saito, T., Imazu, K., Hayashi, T., Derocher, A.E., Wiig, O.: Differences in oligosaccharides pattern of a sample of polar bear colostrum and mid-lactation milk. Comp. Biochem. Physiol. B136, 887–896 (2003)CrossRefGoogle Scholar
  13. 13.
    Urashima, T., Nakamura, T., Teramoto, K., Arai, I., Saito, T., Komatsu, T., Tsubota, T.: Chemical characterization of sialyl oligosaccharides in milk of the Japanese black bear, Ursus thibetanus japonicas. Comp. Biochem. Physiol. 139B, 587–595 (2004)CrossRefGoogle Scholar
  14. 14.
    Nakamura, T., Urashima, T., Mizukami, T., Fukushima, M., Arai, I., Senshu, T., Imazu, K., Nakao, T., Saito, T., Ye, Z., Zuo, H., Wu, K.: Composition and oligosaccharides of a milk sample of the giant panda, Ailuropoda melanoleuca. Comp. Biochem. Physiol. B135, 439–448 (2003)CrossRefGoogle Scholar
  15. 15.
    Urashima, T., Arita, M., Yoshida, M., Nakamura, T., Arai, I., Saito, T., Arnould, J.P.Y., Kovacs, K.M., Lydersen, C.: Chemical characterization of the oligosaccharides in hooded seal. (Cystophora cristata) and Australian fur seal (Arctocephalus pusillus doriferus) milk. Comp. Biochem. Physiol. B128, 307–323 (2001)CrossRefGoogle Scholar
  16. 16.
    Urashima, T., Nakamura, T., Yamaguchi, K., Munakata, J., Arai, I., Saito, T., Lydersen, C., Kovacs, K.M.: Chemical characterization of the oligosaccharides in milk of high Arctic harbour seal (Phoca vitulina vitulina). Comp. Biochem. Physiol. A135, 549–563 (2003)CrossRefGoogle Scholar
  17. 17.
    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)CrossRefGoogle Scholar
  18. 18.
    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)CrossRefPubMedGoogle Scholar
  19. 19.
    Urashima, T., Yamamoto, M., Nakamura, T., Arai, I., Saito, T., Namiki, M., Yamaoka, K., Kawahara, K.: Chemical characterisation of the oligosaccharides in a sample of milk of a white-nosed coati, Nasua narica (Procyonidae: Carnivora). Comp. Biochem. Physiol. A123, 187–193 (1999)CrossRefGoogle Scholar
  20. 20.
    Taufik, E., Sekii, N., Senda, A., Fukuda, K., Saito, T., Eisert, R., Oftedal, O.T., Urashima, T.: Neutral and acidic milk oligosaccharides of the striped skunk (Mephitidae: Mephitis mephitis). Anim. Sci. J. 84, 569–578 (2013)CrossRefPubMedGoogle Scholar
  21. 21.
    Urashima, T., Nakamura, T., Ikeda, A., Asakuma, S., Arai, I., Saito, T., Oftedal, O.T.: Characterization of oligosaccharides in milk of a mink, Mustela vison. Comp. Biochem. Physiol. A142, 461–471 (2005)CrossRefGoogle Scholar
  22. 22.
    Bubb, W.A., Urashima, T., Kohso, K., Nakamura, T., Arai, I., Saito, T.: Occurrence of an unusual lactose sulfate in dog milk. Carbohydr. Res. 318, 123–128 (1999)CrossRefPubMedGoogle Scholar
  23. 23.
    Rostami, M.S., Benet, T., Spears, J., Reynolds, A., Satyaraj, E., Sprenger, N., Austin, S.: Milk oligosaccharides over time of lactation from different dog breeds. PLoS One. e99824 (2014)Google Scholar
  24. 24.
    Uemura, Y., Takahashi, S., Senda, A., Fukuda, K., Saito, T., Oftedal, O.T., Urashima, T.: Chemical characterization of milk oligosaccharides of a spotted hyena (crocuta crocuta). Comp. Biochem. Physiol. A152, 158–161 (2009)CrossRefGoogle Scholar
  25. 25.
    Senda, A., Hatakeyama, E., Kobayashi, R., Fukuda, K., Uemura, Y., Saito, T., Packer, C., Oftedal, O.T., Urashima, T.: Chemical characterization of milk oligosaccharides of an African lion (Panthera leo) and a clouded leopard (Neofelis nebulosa). Anim. Sci. J. 81, 687–693 (2010)CrossRefPubMedGoogle Scholar
  26. 26.
    Dubois, M., Gill, K.A., Hamilton, J.K., Roberts, P.A., Smith, F.: Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–356 (1956)CrossRefGoogle Scholar
  27. 27.
    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
  28. 28.
    Green, B., Merchant, J.C.: The composition of marsupial milk. In: Tyndale Biscoe, C.H., Janssens, P.A. (eds.) The developing marsupial, pp. 41–54. Springer-Verlag, Berlin (1988)CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Food ScienceObihiro University of Agriculture & Veterinary MedicineObihiroJapan
  2. 2.The United Graduate School of Agricultural SciencesIwate UniversityMoriokaJapan
  3. 3.Animal Research Center, Hokkaido Research OrganizationShintokuJapan
  4. 4.Graduate School of AgricultureTohoku UniversitySendai, MiyagiJapan

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