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Chemical characterization of the milk oligosaccharides of some Artiodactyla species including giraffe (Giraffa camelopardalis), sitatunga (Tragelaphus spekii), deer (Cervus nippon yesoensis) and water buffalo (Bubalus bubalis)

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Abstract

Mammalian milk/colostrum usually contains oligosaccharides along with the predominant disaccharide lactose. It has been found that the number and identity of these milk oligosaccharides varies among mammalian species. Oligosaccharides predominate over lactose in the milk/colostrum of Arctoidea species (Carnivora), whereas lactose predominates over milk oligosaccharides in Artiodactyla including cow, sheep, goat, camel, reindeer and pig. To clarify whether heterogeneity of a variety of milk oligosaccharides is found within other species of Artiodactyla, they were studied in the milk of giraffe, sitatunga, deer and water buffalo. The following oligosaccharides were found: Neu5Ac(α2–3)[GalNAc(β1–4)]Gal(β1–4)Glc (GM2 tetrasaccharide), and Gal(α1–3)Gal(β1–4)Glc (isoglobotriose) in giraffe milk; Neu5Ac(α2–3)Gal(β1–4)Glc (3’-SL), Neu5Ac(α2–6)Gal(β1–4)Glc (6’-SL), Gal(α1–4)Gal(β1–4)Glc (globotriose) and isoglobotriose in sitatunga colostrum; Gal(β1–3)Gal(β1–4)Glc (3′-GL), Gal(β1–6)Gal(β1–4)Glc (6′-GL), isoglobotriose, Gal(β1–4)GlcNAc(β1–3)Gal(β1–4)Glc (lacto-N-neotetraose, LNnT), Gal(β1–4)Glc-3’-O-SO3 (3’-O-lactose sulphate) in deer milk; 3′-GL, isoglobotriose and Gal(β1–3)Gal(β1–3)Gal(β1–4)Glc (3′,3″-digalactosyllactose, DGL) in water buffalo colostrum. Thus it was shown that the milk oligosaccharides are heterogeneous among these Artiodactyla species.

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Acknowledgements

We thank to Mr. Katsumasa Tomita of Shiretoko Ezoshika Farm for supplying deer milk. This work was supported by a Grant-in-Aid for Scientific Research ©, 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). We thank Directorate of Higher Education of Republic Indonesia through foreign collaboration research scheme 2018 for supporting the collection and analysis of water buffalo colostrum.

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Authors and Affiliations

  1. Department of Life and Food Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555, Japan

    Yuri Mineguchi, Midori Miyoshi, Kenji Fukuda & Tadasu Urashima

  2. Faculty of Animal Science, Bogor Agricultural University, Bogor, 16680, Indonesia

    Epi Taufik

  3. Kyoto City Zoo, Kyoto, 606-8333, Japan

    Ayumi Kawamura

  4. Himeji Central Park, Himeji, Hyogo, 679-2121, Japan

    Takuya Asakawa & Isao Suzuki

  5. Department of Northern Biosphere Agriculture, Faculty of Bioindustry, Tokyo University of Agriculture, Abashiri, Hokkaido, 099-2493, Japan

    Kousaku Souma & Michiko Okubo

  6. Graduate School of Agriculture, Tohoku University, Sendai, Miyagi, 980-0845, Japan

    Tadao Saito

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

    Sadaki Asakuma

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  1. Yuri Mineguchi
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Supplementary Fig. 1

Thin layer chromatogram of the fractions of SCG-4, SC-4, D-5 and B-4 separated from milk or colostrum of giraffe, sitatunga, deer and water buffalo, respectively, by gel filtration on BioGel P-2 (see Fig. 1). Acetone/2-propanol/0.1 mol lactic acid (2:2:1, v/v/v) was used as a developing solvent. Detection of the spots was done by spraying with 5% H2SO4 in ethanol and heating. The lanes are as follows: a, authentic lactose; b, SCG-4; c, SC-4; d, D-5; e, B-4. (PDF 97 kb)

Supplementary Fig. 2

1H-NMR spectrum of the oligosaccharide in fraction of SCG-1_10 separated from giraffe milk (see Fig. 2a). The spectrum was obtained in D2O at 600 MHz with a Varian INOVA 600 spectrometer operated at 293 K. Chemical shifts are expressed relative to internal 3-(trimethylsilyl)-1-propane sulfuric acid, sodium salt, but were actually measured by reference to internal acetone (δ = 2.225). (PDF 176 kb)

Supplementary Fig. 3

Matrix-assisted, laser-desorption time-of-flight mass spectrum of the oligosaccharide in fraction of SCG-1_10. The mass spectrometry was performed using an Autoflex II TOF/TOF mass spectrometer (Brucker Daltonics, Bremen, Germany). Lyophilized oligosaccharide fractions were dissolved in 1 μL of milli-Q water. The oligosaccharide solution was mixed with an equal volume of 10 mg/mL. SDHB (Brucker Daltonics), which is a mixture of 2,5-dihydrobenzoic acid and 2-hydroxy-5-methoxybenzoic acid, saturated in milli-Q water, spotted on a MTP 384 target plate ground steel TF (Bruker Daltnics), and dried. Mass spectra were obtained using a pre-installed method, RP_0–2 kDa (a reflector positive ion mode focusing on the mass range up to 2 kDa). (PDF 98 kb)

Supplementary Fig. 4

1H-NMR spectrum of the oligosaccharide in fraction of SC-3 separated from sitatunga colostrum (see Fig. 1b). The spectrum was obtained in D2O at 500 MHz with a JEOL ECP-500 Fourier transform-NMR spectrometer operated at 293 K. (PDF 163 kb)

Supplementary Fig. 5

1H-NMR spectrum of the oligosaccharide in fraction of SC-1_1 separated from sitatunga colostrum (see Fig. 3a). The spectrum was obtained in D2O at at 600 MHz with a Varian INOVA 600 spectrometer operated at 293 K. (PDF 183 kb)

Supplementary Fig. 6

Matrix-assisted, laser-desorption time-of-flight mass spectrum of the oligosaccharide in fraction of SC-1_1. (PDF 87 kb)

Supplementary Fig. 7

1H-NMR spectrum of the oligosaccharide in fraction of D-4 separated from deer milk (see Fig. 1c). The spectrum was obtained in D2O at 500 MHz with a JEOL ECP-500 Fourier transform-NMR spectrometer operated at 293 K. (PDF 272 kb)

Supplementary Fig. 8

1H-NMR spectrum of the oligosaccharide in fraction of B-2_10 separated from water buffalo colostrum (see Fig. 4a). The spectrum was obtained in D2O at 500 MHz with a JEOL ECP-500 Fourier transform-NMR spectrometer operated at 293 K. (PDF 222 kb)

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Mineguchi, Y., Miyoshi, M., Taufik, E. et al. Chemical characterization of the milk oligosaccharides of some Artiodactyla species including giraffe (Giraffa camelopardalis), sitatunga (Tragelaphus spekii), deer (Cervus nippon yesoensis) and water buffalo (Bubalus bubalis). Glycoconj J 35, 561–574 (2018). https://doi.org/10.1007/s10719-018-9849-0

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