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http://dx.doi.org/10.5851/kosfa.2022.e13

Characterization of Bioactive Sialyl Oligosaccharides Separated from Colostrum of Indonesia Dairy Goat  

Taufik, Epi (Department of Animal Production and Technology, Faculty of Animal Science, IPB University)
Arief, Irma Isnafia (Department of Animal Production and Technology, Faculty of Animal Science, IPB University)
Budiman, Cahyo (Department of Animal Production and Technology, Faculty of Animal Science, IPB University)
Wibisono, Yusuf (Department of Bioprocess Engineering, Brawijaya University)
Noviyanto, Alfian (Department of Mechanical Engineering, Mercu Buana University)
Publication Information
Food Science of Animal Resources / v.42, no.3, 2022 , pp. 426-440 More about this Journal
Abstract
The bioactive functions of oligosaccharides from human milk have been reported by many studies. Many of oligosaccharides isolated from colostrum and/or milk of dairy animals have been reported to have similar chemical structures with those in human colostrum and/or milk. It has been proved by several studies that the oligosaccharides with similar chemical structure shared common bioactivities. Among domesticated dairy animals, bovine/cattle, caprine/goat, and ovine/sheep are the most commonly used species to isolate oligosaccharides from their colostrum and/or milk. Several studies on the oligosaccharides from goat colostrum and milk have revealed similar properties to that of human milk and possess the highest content of sialyl oligosaccharides (SOS) as compared to other ruminants. Indonesia ranks first in Association of Southeast Asian Nations (ASEAN) for goat milk production. Therefore, goat milk is the second most consumed milk in the country. The most reared dairy goat breed in Indonesia is Etawah Grade. However, oligosaccharides from Indonesia dairy animals including goat, have not been characterized. This is the first study to characterize oligosaccharides from Indonesia dairy animals. The present study was aimed to isolate and characterize oligosaccharides, specifically SOS from the colostrum of Etawah Grade goats by using proton/1H-nuclear magnetic resonance. The SOS successfully characterized in this study were: Neu5Ac(α2-3)Gal(β1-4)Glc (3'-N-acetylneuraminyllactose), Neu5Ac(α2-6)Gal(β1-4)Glc (6'-N-acetylneuraminyllactose), Neu5Gc(α2-3)Gal(β1-4)Glc (3'-N-glycolylneuraminyllactose), Neu5Gc(α2-6)Gal(β1-4)Glc (6'-N-glycolylneuraminyllactose), Neu5Ac(α2-6)Gal(β1-4) GlcNAc (6'-N-acetylneuraminyllactosamine) and Neu5Gc(α2-6)Gal(β1-4)GlcNAc (6'-N-glycolylneuraminyllactosamine). This finding shows that Etawah Grade, as a local dairy goat breed in Indonesia, is having significant potential to be natural source of oligosaccharides that can be utilized in the future food and pharmaceutical industries.
Keywords
oligosaccharides; colostrum; milk; Etawah Grade; dairy goat;
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1 Urashima T, Saito T, Nakamura T, Messer M. 2001. Oligosaccharides of milk and colostrum in non-human mammals. Glycoconj J 18:357-371.   DOI
2 Urashima T, Taufik E. 2010. Oligosaccharides in milk: Their benefits and future utilization. Media Peternakan 33:189.   DOI
3 Newburg DS, Neubauer SH. 1995. Carbohydrates in milks: Analysis, quantities and significance. In Handbook of milk composition. Jensen RG (ed). Academic Press, San Diego, CA, USA. pp 273-349.
4 Perret S, Sabin C, Dumon C, Pokorna M, Gautier C, Galanina O, Ilia S, Bovin N, Nicaise M, Desmadril M, Gilboa-Garber N, Wimmerova M, Mitchell EP, Imberty A. 2005. Structural basis for the interaction between human milk oligosaccharides and the bacterial lectin PA-IIL of Pseudomonas aeruginosa. Biochem J 389:325-332.   DOI
5 Bode L. 2012. Human milk oligosaccharides: Every baby needs a sugar mama. Glycobiology 22:1147-1162.   DOI
6 van Leeuwen SS, Te Poele EM, Chatziioannou AC, Benjamins E, Haandrikman A, Dijkhuizen L. 2020. Goat milk oligosaccharides: Their diversity, quantity, and functional properties in comparison to human milk oligosaccharides. J Agric Food Chem 68:13469-13485.   DOI
7 Viverge D, Grimmonprez L, Solere M. 1997. Chemical characterization of sialyl oligosaccharides isolated from goat (Capra hircus) milk. Biochim Biophys Acta 1336:157-164.   DOI
8 Zopf D, Roth S. 1996. Oligosaccharide anti-infective agents. Lancet 347:1017-1021.   DOI
9 Albrecht S, Lane JA, Marino K, Al Busadah KA, Carrington SD, Hickey RM, Rudd PM. 2014. A comparative study of free oligosaccharides in the milk of domestic animals. Br J Nutr 111:1313-1328.   DOI
10 Alhaj OA, Taufik E, Handa Y, Fukuda K, Saito T, Urashima T. 2013. Chemical characterisation of oligosaccharides in commercially pasteurised dromedary camel (Camelus dromedarius) milk. Int Dairy J 28:70-75.   DOI
11 Bode L, Kunz C, Muhly-Reinholz M, Mayer K, Seeger W, Rudloff S. 2004. Inhibition of monocyte, lymphocyte, and neutrophil adhesion to endothelial cells by human milk oligosaccharides. Thromb Haemost 92:1402-1410.   DOI
12 Boehm G, Stahl B. 2007. Oligosaccharides from milk. J Nutr 137:Suppl 2:S847-S849.
13 Claps S, Di Napoli MA, Caputo AR, Rufrano D, Sepe L, Di Trana A. 2016. Factor affecting the 3' sialyllactose, 6' sialyllactose and disialyllactose content in caprine colostrum and milk: Breed and parity. Small Rumin Res 134:8-13.   DOI
14 Crane JK, Azar SS, Stam A, Newburg DS. 1994. Oligosaccharides from human milk block binding and activity of the Escherichia coli heat-stable enterotoxin (STa) in T84 intestinal cells. J Nutr 124:2358-2364.   DOI
15 Daddaoua A, PuertaV, Requena P, Martinez-Ferez A, Guadix E, de Medina FS, Zarzuelo A, Suarez MD, Boza JJ, MartinezAugustin O. 2006. Goat milk oligosaccharides are anti-inflammatory in rats with hapten-induced colitis. Nutr Immun 136:672-676.
16 Sousa YRF, Araujo DFS, Pulido JO, Pintado MME, Martinez-Ferez A, Queiroga RCRE. 2019a. Composition and isolation of goat cheese whey oligosaccharides by membrane technology. Int J Biol Macromol 139:57-62.   DOI
17 Plaza-Diaz J, Fontana L, Gil A. 2018. Human milk oligosaccharides and immune system development. Nutrients 10:1038.   DOI
18 Saito T, Itoh T, Adachi S. 1984. Presence of two neutral disaccharides containing N-acetylhexosamine in bovine colostrum as free forms. Biochim Biophys Acta 801:147-150.   DOI
19 Saito T, Itoh T, Adachi S. 1987. Chemical structure of three neutral trisaccharides isolated in free form from bovine colostrum. Carbohydr Res 165:43-51.   DOI
20 Nakamura T, Kawase H, Kimura K, Watanabe Y, Ohtani M, Arai I, Urashima T. 2003. Concentrations of sialyloligosaccharides in bovine colostrum and milk during the prepartum and early lactation. J Dairy Sci 86:1315-1320.   DOI
21 Oliveira DL, Wilbey RA, Grandison AS, Roseiro LB. 2015. Milk oligosaccharides: A review. Int J Dairy Technol 68:305-321.   DOI
22 Taufik E, Ganzorig K, Nansalmaa M, Fukuda R, Fukuda K, Saito T, Urashima T. 2014. Chemical characterisation of saccharides in the milk of a reindeer (Rangifer tarandus tarandus). Int Dairy J 34:104-108.   DOI
23 Sundekilde UK, Barile D, Meyrand M, Poulsen NA, Larsen LB, Lebrilla CB, German JB, Bertram HC. 2012. Natural variability in bovine milk oligosaccharides from Danish Jersey and Holstein-Friesian breeds. J Agric Food Chem 60:6188-6196.   DOI
24 Urakami H, Saeki M, Watanabe Y, Kawamura R, Nishizawa S, Suzuki Y, Watanabe A, Ajisaka K. 2018. Isolation and assessment of acidic and neutral oligosaccharides from goat milk and bovine colostrum for use as ingredients of infant formulae. Int Dairy J 83:1-9.   DOI
25 Urashima T, Bubb WA, Messer M, Tsuji Y, Taneda Y. 1994. Studies of the neutral trisaccharides of goat (Capra hircus) colostrum and of the one- and two-dimensional 1 H and 13C NMR spectra of 6'-N-acetylglucosaminyllactose. Carbohydr Res 262:173-184.   DOI
26 Martin-Ortiz A, Barile D, Salcedo J, Moreno FJ, Clemente A, Ruiz-Matute AI, Sanz ML. 2017. Changes in caprine milk oligosaccharides at different lactation stages analyzed by high performance liquid chromatography coupled to mass spectrometry. J Agric Food Chem 65:3523-3531.   DOI
27 Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS. 2003. Campylobacter jejuni binds intestinal H(O) antigen (Fucα1, 2Galβ1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 278:14112-14120.   DOI
28 Sasaki M, Nakamura T, Hirayama K, Fukuda K, Saito T, Urashima T, Asakuma S. 2016. Characterization of two novel sialyl N-acetyllactosaminyl nucleotides separated from ovine colostrum. Glycoconj J 33:789-796.   DOI
29 Sousa YRF, Medeiros LB, Pintado MME, Queiroga RCRE. 2019b. Goat milk oligosaccharides: Composition, analytical methods and bioactive and nutritional properties. Trends Food Sci Technol 92:152-161.   DOI
30 Urashima T, Murata S, Nakamura T. 1997. Structural determination of monosialyl trisaccharides obtained from caprine colostrum. Comp Biochem Physiol B Biochem Mol Biol 116:431-435.   DOI
31 Urashima T, Taufik E, Fukuda K, Asakuma S. 2013. Recent advances in studies on milk oligosaccharides of cows and other domestic farm animals. Biosci Biotechnol Biochem 77:455-466.   DOI
32 Yue H, Han Y, Yin B, Cheng C, Liu L. 2020. Comparison of the antipathogenic effect toward Staphylococcus aureus of N-linked and free oligosaccharides derived from human, bovine, and goat milk. J Food Sci 85:2329-2339.   DOI
33 Leong A, Liu Z, Almshawit H, Zisu B, Pillidge C, Rochfort S, Gill H. 2019. Oligosaccharides in goats' milk-based infant formula and their prebiotic and anti-infection properties. Br J Nutr 122:441-449.   DOI
34 Newburg DS. 2000. Oligosaccharides in human milk and bacterial colonization. J Pediatr Gastroenterol Nutr 30:Suppl 2:S8-S17.
35 Food and Agriculture Organization (FAO). 2021. FAO stat. Available from: https://www.fao.org/faostat/en/#data/QCL. Accessed at Nov 19, 2021.
36 Barile D, Marotta M, Chu C, Mehra R, Grimm R, Lebrilla CB, German JB. 2010. Neutral and acidic oligosaccharides in Holstein-Friesian colostrum during the first 3 days of lactation measured by high performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry. J Dairy Sci 93:3940-3949.   DOI
37 Claps S, Di Napoli MA, Sepe L, Caputo AR, Rufrano D, Di Trana A, Annicchiarico G, Fedele V. 2014. Sialyloligosaccharides content in colostrum and milk of two goat breeds. Small Rumin Res 121:116-119.   DOI
38 Fukuda K, Yamamoto A, Ganzorig K, Khuukhenbaatar J, Senda A, Saito T, Urashima T. 2010. Chemical characterization of the oligosaccharides in Bactrian camel (Camelus bactrianus) milk and colostrum. J Dairy Sci 93:5572-5587.   DOI
39 Huang Z, Li Y, Luo Y, Guo H. 2021. Human milk oligosaccharides 3'-sialyllactose and 6'-sialyllactose protect intestine against necrotizing enterocolitis damage induced by hypoxia. J Funct Foods 86:104708.   DOI
40 Kunz C, Kuntz S, Rudloff S. 2014. Bioactivity of human milk oligosaccharides. In Food oligosaccharides: Production, analysis and bioactivity. Moreno FJ, Sanz ML (ed). John Wiley & Sons, London, UK. pp 1-20.
41 Meyrand M, Dallas DC, Caillat H, Bouvier F, Martin P, Barile D. 2013. Comparison of milk oligosaccharides between goats with and without the genetic ability to synthesize αs1-casein. Small Rumin Res 113:411-420.   DOI
42 Newburg DS, Ko JS, Leone S, Nanthakumar NN. 2016. Human milk oligosaccharides and synthetic galactosyloligosaccharides contain 3'-, 4-, and 6'-galactosyllactose and attenuate inflammation in human T84, NCM-460, and H4 cells and intestinal tissue ex vivo. J Nutr 146:358-367.   DOI
43 Silanikove N, Leitner G, Merin U, Prosser CG. 2010. Recent advances in exploiting goat's milk: Quality, safety and production aspects. Small Rumin Res 89:110-124.   DOI
44 Taufik E, Fukuda K, Senda A, Saito T, Williams C, Tilden C, Eisert R, Oftedal O, Urashima T. 2012. Structural characterization of neutral and acidic oligosaccharides in the milks of strepsirrhine primates: Greater galago, aye-aye, Coquerel's sifaka and mongoose lemur. Glycoconj J 29:119-134.   DOI
45 Martinez-Ferez A, Rudloff S, Guadix A, Henkel CA, Pohlentz G, Boza JJ, Guadix EM, Kunz C. 2006b. Goats' milk as a natural source of lactose-derived oligosaccharides: Isolation by membrane technology. Int Dairy J 16:173-181.   DOI
46 Martin-Sosa S, Martin MJ, Garcia-Pardo LA, Hueso P. 2003. Sialyloligosaccharides in human and bovine milk and in infant formulas: Variations with the progression of lactation. J Dairy Sci 86:52-59.   DOI
47 Nakamura T, Urashima T, Nakagawa M, Saito T. 1998. Sialyllactose occurs as free lactones in ovine colostrum. Biochim Biophys Acta 1381:286-292.   DOI
48 Newburg DS. 1999. Human milk glycoconjugates that inhibit pathogens. Curr Med Chem 6:117-127.   DOI
49 Badan Pusat Statistik [BPS]. 2021. Populasi Kambing menurut Provinsi (Ekor), 2019-2021. Available from: https://www.bps.go.id/indicator/24/472/1/populasi-kambing-menurut-provinsi.html. Accessed at Nov 19, 2021.
50 Ganzorig K, Asakawa T, Sasaki M, Saito T, Suzuki I, Fukuda K, Urashima T. 2018. Identification of sialyl oligosaccharides including an oligosaccharide nucleotide in colostrum of an addax (Addax nasomaculatus) (Subfamily Antelopinae). Anim Sci J 89:167-175.   DOI
51 Bode L, Jantscher-Krenn E. 2012. Structure-function relationships of human milk oligosaccharides. Adv Nutr 3:S383-S391.
52 Chatziioannou AC, Benjamins E, Pellis L, Haandrikman A, Dijkhuizen L, van Leeuwen SS. 2021. Extraction and quantitative analysis of goat milk oligosaccharides: Composition, variation, associations, and 2'-FL variability. J Agric Food Chem 69:7851-7862.   DOI
53 Lane JA, Mehra RK, Carrington SD, Hickey RM. 2010. The food glycome: A source of protection against pathogen colonization in the gastrointestinal tract. Int J Food Microbiol 142:1-13.   DOI
54 Lu J, Zhang Y, Song B, Zhang S, Pang X, Sari RN, Liu L, Wang J, Lv J. 2020. Comparative analysis of oligosaccharides in Guanzhong and Saanen goat milk by using LC-MS/MS. Carbohydr Polym 235:115965.   DOI
55 Martinez-Ferez A, Guadix A, Guadix EM. 2006a. Recovery of caprine milk oligosaccharides with ceramic membranes. J Membr Sci 276:23-30.   DOI
56 Gopal PK, Gill HS. 2000. Oligosaccharides and glycoconjugates in bovine milk and colostrum. Br J Nutr 84:Suppl 1:S69-S74.   DOI
57 Martin-Ortiz A, Salcedo J, Barile D, Bunyatratchata A, Moreno FJ, Martin-Garcia I, Clemente A, Sanz ML, Ruiz-Matute AI. 2016. Characterization of goat colostrum oligosaccharides by nano-liquid chromatography on chip quadrupole time-offlight mass spectrometry and hydrophilic interaction liquid chromatography-quadrupole mass spectrometry. J Chromatogr A 1428:143-153.   DOI
58 Coppa GV, Zampini L, Galeazzi T, Facinelli B, Ferrante L, Capretti R, Orazio G. 2006. Human milk oligosaccharides inhibit the adhesion to Caco-2 cells of diarrheal pathogens: Escherichia coli, Vibrio cholerae, and Salmonella fyris. Pediatr Res 59:377-382.   DOI
59 DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal Chem 28:350-356.   DOI
60 Jourdian GW, Dean L, Roseman S. 1971. The sialic acids: XI. A periodate-resorcinol method for the quantitative estimation of free sialic acids and their glycosides. J Biol Chem 246:430-435.   DOI
61 Kiskini A, Difilippo E. 2013. Oligosaccharides in goat milk: Structure, health effects and isolation. Cell Mol Biol 59:25-30.
62 Lane JA, Marino K, Rudd PM, Carrington SD, Slattery H, Hickey RM. 2012. Methodologies for screening of bacteria-carbohydrate interactions: Anti-adhesive milk oligosaccharides as a case study. J Microbiol Methods 90:53-59.   DOI